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• W2129335564 abstract "In previous studies, we characterized five histidine kinases (Hiks) and the cognate response regulators (Rres) that control the expression of ∼70% of the hyperosmotic stress-inducible genes in the cyanobacterium Synechocystis sp. PCC 6803. In the present study, we screened a gene knock-out library of Rres by RNA slot-blot hybridization and with a genome-wide DNA microarray and identified three Hik-Rre systems, namely, Hik33-Rre31, Hik10-Rre3, and Hik16-Hik41-Rre17, as well as another system that included Rre1, that were involved in perception of salt stress and transduction of the signal. We found that these Hik-Rre systems were identical to those that were involved in perception and transduction of the hyperosmotic stress signal. We compared the induction factors of the salt stress- and hyperosmotic stress-inducible genes that are located downstream of each system and found that these genes responded to the two kinds of stress to different respective extents. In addition, the Hik33-Rre31 system regulated the expression of genes that were specifically induced by hyperosmotic stress, whereas the system that included Rre1 regulated the expression of one or two genes that were specifically induced either by salt stress or by hyperosmotic stress. Our observations suggest that the perception of salt and hyperosmotic stress by the Hik-Rre systems is complex and that salt stress and hyperosmotic stress are perceived as distinct signals by the Hik-Rre systems. In previous studies, we characterized five histidine kinases (Hiks) and the cognate response regulators (Rres) that control the expression of ∼70% of the hyperosmotic stress-inducible genes in the cyanobacterium Synechocystis sp. PCC 6803. In the present study, we screened a gene knock-out library of Rres by RNA slot-blot hybridization and with a genome-wide DNA microarray and identified three Hik-Rre systems, namely, Hik33-Rre31, Hik10-Rre3, and Hik16-Hik41-Rre17, as well as another system that included Rre1, that were involved in perception of salt stress and transduction of the signal. We found that these Hik-Rre systems were identical to those that were involved in perception and transduction of the hyperosmotic stress signal. We compared the induction factors of the salt stress- and hyperosmotic stress-inducible genes that are located downstream of each system and found that these genes responded to the two kinds of stress to different respective extents. In addition, the Hik33-Rre31 system regulated the expression of genes that were specifically induced by hyperosmotic stress, whereas the system that included Rre1 regulated the expression of one or two genes that were specifically induced either by salt stress or by hyperosmotic stress. Our observations suggest that the perception of salt and hyperosmotic stress by the Hik-Rre systems is complex and that salt stress and hyperosmotic stress are perceived as distinct signals by the Hik-Rre systems. Responses to salt stress and hyperosmotic stress have been investigated in prokaryotes, fungi, and plants. However, there is some confusion in the literature because salt stress and hyperosmotic stress have been regarded both as equivalent and as distinct stimuli (1van Wuytswinkel O. Reiser V. Siderius M. Kelders M.C. Ammerer G. Ruis H. Mager W.H. Mol. Microbiol. 2000; 37: 382-397Crossref PubMed Scopus (96) Google Scholar, 2Figge R.M. Cassier-Chauvat C. Chauvat F. Cerff R. Mol. Microbiol. 2001; 39: 455-468Crossref PubMed Scopus (82) Google Scholar, 3Kanesaki Y. Suzuki I. Allakhverdiev S.I. Mikami K. Murata N. Biochem. Biophys. Res. Commun. 2002; 290: 339-348Crossref PubMed Scopus (242) Google Scholar, 4Kreps J.A. Wu Y. Chang H.S. Zhu T. Wang X. Harper J.F. Plant Physiol. 2002; 130: 2129-2141Crossref PubMed Scopus (1190) Google Scholar). In Arabidopsis thaliana, both salt stress due to 0.1 m NaCl and hyperosmotic stress due to 0.2 m mannitol regulate the expression of not only the same set of genes but also of different sets of genes (4Kreps J.A. Wu Y. Chang H.S. Zhu T. Wang X. Harper J.F. Plant Physiol. 2002; 130: 2129-2141Crossref PubMed Scopus (1190) Google Scholar). In the cyanobacterium Synechocystis sp. PCC 6803 (hereafter, Synechocystis), it is clear that there are major differences between the sets of genes that respond to salt stress due to 0.5 m NaCl and hyperosmotic stress due to 0.5 m sorbitol (3Kanesaki Y. Suzuki I. Allakhverdiev S.I. Mikami K. Murata N. Biochem. Biophys. Res. Commun. 2002; 290: 339-348Crossref PubMed Scopus (242) Google Scholar). Moreover, the cytoplasmic volume of Synechocystis decreases by ∼70% of the original volume within 10 min when cells are exposed to 0.5 m sorbitol, but the decrease in cytoplasmic volume is only 30% with 0.5 m NaCl (3Kanesaki Y. Suzuki I. Allakhverdiev S.I. Mikami K. Murata N. Biochem. Biophys. Res. Commun. 2002; 290: 339-348Crossref PubMed Scopus (242) Google Scholar). Although the responses to hyperosmotic stress and salt stress are different in terms of gene expression and changes in cytoplasmic volume, recent studies have demonstrated that the same histidine kinases (Hiks), 1The abbreviations used are: Hik, histidine kinase; Rre, response regulator; ORF, open reading frame; RE, effective ratio.1The abbreviations used are: Hik, histidine kinase; Rre, response regulator; ORF, open reading frame; RE, effective ratio. such as Hik33, Hik34, and Hik16, might be involved in the perception of salt and hyperosmotic stress (5Marin K. Suzuki I. Yamaguchi K. Ribbeck K. Yamamoto H. Kanesaki Y. Hagemann M. Murata N. Proc. Natl. Acad. Sci. U. S. A. 2003; 100: 9061-9066Crossref PubMed Scopus (136) Google Scholar, 6Paithoonrangsarid K. Shoumskaya M.A. Kanesaki Y. Satoh S. Tabata S. Los D.A. Zinchenko V.V. Hayashi H. Tanticharoen M. Suzuki I. Murata N. J. Biol. Chem. 2004; 279: 53078-53086Abstract Full Text Full Text PDF PubMed Scopus (107) Google Scholar). In Synechocystis, several Hiks that are paired with specific response regulators (Rres) have been identified as regulators of the response to hyperosmotic stress (6Paithoonrangsarid K. Shoumskaya M.A. Kanesaki Y. Satoh S. Tabata S. Los D.A. Zinchenko V.V. Hayashi H. Tanticharoen M. Suzuki I. Murata N. J. Biol. Chem. 2004; 279: 53078-53086Abstract Full Text Full Text PDF PubMed Scopus (107) Google Scholar). A specific Hik senses hyperosmotic stress, and it seems likely that the signal is transferred to the cognate Rre by transfer of a phosphate group from the histidine residue of the Hik to an aspartate residue in the receiver domain of the Rre, which in turn acts either to derepress or to induce the expression of downstream genes. Screenings using yeast two-hybrid systems (7Fields S. Song O. Nature. 1989; 340: 245-246Crossref PubMed Scopus (4799) Google Scholar) have also provided evidence for the physical interactions between respective members of cognate pairs of Hiks and Rres. The genome of Synechocystis encodes 47 Hiks and 45 Rres (Refs. 8Kaneko 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. DNA Res. 1996; 3: 109-136Crossref PubMed Scopus (2100) Google Scholar and 9Kaneko T. Nakamura Y. Sasamoto S. Watanabe A. Kohara M. Matsumoto M. Shimpo S. Yamada M. Tabata S. DNA Res. 2003; 10: 221-228Crossref PubMed Scopus (102) Google Scholar; see also www.kazusa.or.jp/cyanobase/Synechocystis/index.html). We have constructed libraries of knockout mutants of these genes as part of a program aimed at elucidating the specific combinations of Hiks and Rres that are associated with the perception and transduction of a variety of stress signals. A previous study demonstrated that Hik33, which was identified first as a cold sensor (10Suzuki I. Kanesaki Y. Mikami K. Kanehisa M. Murata N. Mol. Microbiol. 2001; 40: 235-244Crossref PubMed Scopus (197) Google Scholar), is also involved in perception of hyperosmotic stress (11Mikami K. Kanesaki Y. Suzuki I. Murata N. Mol. Microbiol. 2002; 46: 905-915Crossref PubMed Scopus (156) Google Scholar). Studies involving systematic mutagenesis of Hiks and Rres in conjunction with DNA microarray analysis have demonstrated that Hik34, Hik10, and a combination of Hik16 plus Hik41 are also involved in perception of hyperosmotic stress. We have identified the Rres located downstream of the Hiks in the pathway for transduction of the hyperosmotic stress signal (6Paithoonrangsarid K. Shoumskaya M.A. Kanesaki Y. Satoh S. Tabata S. Los D.A. Zinchenko V.V. Hayashi H. Tanticharoen M. Suzuki I. Murata N. J. Biol. Chem. 2004; 279: 53078-53086Abstract Full Text Full Text PDF PubMed Scopus (107) Google Scholar). The specific cognate partners in the sensing of hyperosmotic stress are Hik33-Rre31, Hik10-Rre3, Hik34-Rre1, Hik16-Hik41-Rre17, and possibly Hik2-Rre1. The histidine kinases Hik33, Hik34, Hik16, and Hik41 have also been identified as components of salt signal-sensing and transducing systems (11Mikami K. Kanesaki Y. Suzuki I. Murata N. Mol. Microbiol. 2002; 46: 905-915Crossref PubMed Scopus (156) Google Scholar). However, we do not know how many salt-responsive genes they might regulate, and the specific Rre associated with each Hik remains to be identified. It is possible that other Hiks might be involved in the sensing of salt stress that have not yet been discovered because of our limited understanding of the way the entire genome responds to salt stress. The responses of the entire genome can be monitored by DNA microarray analysis. A better understanding of the responsiveness of each gene to mutations in specific Hiks would allow us to identify the Hik that is associated with each stress-responsive gene and to identify genes that are not responsive to Hiks that have already been identified and must, thus, be controlled by unidentified factors. In the present study, we identified Hik10 and Hik2 as possibly novel salt-sensing Hiks, as well as the cognate Rres of Hik33, Hik34, Hik16, and Hik41. We compared salt-induced genes with hyperosmotic stress-induced genes and found that the two kinds of stress induced the expression of individual genes to different extents. Our findings demonstrate that the individual systems for recognition of salt stress and hyperosmotic stress are shared, but the two kinds of stress are perceived as different signals. Strains and Culture Conditions—Synechocystis sp. PCC 6803, a glucose-tolerant stain, was kindly provided by Dr. J. G. K. Williams (E. I. du Pont de Nemours & Co., Wilmington, DE), and a glucose-sensitive strain was obtained from Professor S. Shestakov (Department of Genetics, Moscow State University, Russia). These two strains served as wild-type strains for construction of the gene knock-out libraries of Hiks and Rres, as described previously (Refs. 6Paithoonrangsarid K. Shoumskaya M.A. Kanesaki Y. Satoh S. Tabata S. Los D.A. Zinchenko V.V. Hayashi H. Tanticharoen M. Suzuki I. Murata N. J. Biol. Chem. 2004; 279: 53078-53086Abstract Full Text Full Text PDF PubMed Scopus (107) Google Scholar, 12Suzuki I. Los D.A. Kanesaki Y. Mikami K. Murata N. EMBO J. 2000; 19: 1327-1334Crossref PubMed Scopus (215) Google Scholar; see also www.kazusa.or.jp/cyanobase/Synechocystis/mutants/). Wild-type cells were grown photoautotrophically at 34 °C in 50 ml of BG-11 medium buffered with 20 mm HEPES-NaOH (pH 7.5) under continuous illumination from incandescent lamps at 70 microeinstein m-2s-1, with aeration by air that contained 1% CO2, as described previously (13Wada H. Murata N. Plant Cell Physiol. 1989; 30: 971-978Crossref Scopus (44) Google Scholar). Mutant cells were grown under the same conditions as wild-type cells except in the case of precultures, in which BG-11 medium was supplemented with an antibiotic (20 μg ml-1 spectinomycin or 25 μg ml-1 kanamycin for cells in which the genome had been mutated by insertion of a spectinomycin-resistance gene cassette or a kanamycin-resistance gene cassette, respectively). For exposure of cells to salt stress, a solution of 5.0 m NaCl was added to 50 ml of a suspension of cells that had been grown under standard conditions for 16 h, to give a final concentration of 0.5 m. The duration of incubation under salt stress was 20 min, the same duration and molar concentration (of sorbitol) used for the experiments with hyperosmotic stress. Isolation of RNA—After incubation of cultures under designated conditions, 50-ml aliquots were rapidly combined with an equal volume of ice-cold ethanol that contained 5% (w/v) phenol for instantaneous killing of cells and to prevent degradation of mRNA. After collection of the killed cells by centrifugation at 1,000 × g for 5 min at 4 °C, total RNA was isolated by the hot phenol method as described previously (14Kiseleva L.L. Serebriiskaya T.S. Horvath I. Vigh L. Lyukevich A.A. Los D.A. J. Mol. Microbiol. Biotechnol. 2000; 3: 331-338Google Scholar). The extracted RNA was treated with DNase I (Nippon Gene, Tokyo, Japan) to remove contaminating DNA and then purified with a mixture of phenol, chloroform, and isoamyl alcohol (25:24:1, v/v) and precipitated in ethanol. RNA Slot-blot Hybridization and Northern Blotting—For RNA slot-blot hybridization (15Sambrook J. Fritsch E.F. Maniatis T. Molecular Cloning: a Laboratory Manual. 2nd Ed. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY1989: 7.53-7.55Google Scholar), 10 μg of total RNA were applied to a Hybond-N+ nylon membrane (Amersham Biosciences). The RNA on the membrane was allowed to hybridize with a specific probe that had been generated from a salt stress-inducible gene, such as slr1544, dnaK2 (sll0170), slr0967, or ndhR (sll1594). For Northern blotting, 15 μg of total RNA were fractionated by electrophoresis on a 1.2% agarose gel that contained 2.05 m formaldehyde. The RNA was transferred to a Hybond-N+ nylon membrane by capillary transfer and allowed to hybridize with a specific probe. Labeling, hybridization, and washing were performed as described in instructions supplied with the AlkPhos Direct labeling and detection system with CDP-star (Amersham Biosciences). DNA probes were conjugated with alkaline phosphatase (Alkphos Direct kit). After hybridization and washing, blots were soaked in CDP-star solution (Amersham Biosciences), and signals from hybridized transcripts were detected with a luminescence image analyzer (LAS-1000; Fuji-Photo Film, Tokyo, Japan). Blots were also probed with the gene for 16 S rRNA as a control. DNA Microarray Analysis—Synechocystis DNA microarrays (Cyano-CHIP) were purchased from TaKaRa Bio Co. Ltd. (Ohtsu, Japan), and genome-wide analysis of gene expression was performed as described previously (3Kanesaki Y. Suzuki I. Allakhverdiev S.I. Mikami K. Murata N. Biochem. Biophys. Res. Commun. 2002; 290: 339-348Crossref PubMed Scopus (242) Google Scholar, 10Suzuki I. Kanesaki Y. Mikami K. Kanehisa M. Murata N. Mol. Microbiol. 2001; 40: 235-244Crossref PubMed Scopus (197) Google Scholar). All experiments were performed with CyanoCHIP version 1.6, which included 3074 of the 3264 genes on the Synechocystis chromosome. Results were quantified with the IMAGENE version 5.5 program (BioDiscovery, El Segundo, CA). Changes in the levels of transcripts of individual genes relative to the total level of mRNA were calculated after normalization by reference to the total intensity of signals from all genes with the exception of genes for rRNAs. The expression of genes in wild-type cells under salt stress was analyzed in four independent experiments. The expression of genes in Hik mutant cells was analyzed in two independent experiments. Calculations of induction factors and the identification of salt stress-inducible genes were performed as described previously (5Marin K. Suzuki I. Yamaguchi K. Ribbeck K. Yamamoto H. Kanesaki Y. Hagemann M. Murata N. Proc. Natl. Acad. Sci. U. S. A. 2003; 100: 9061-9066Crossref PubMed Scopus (136) Google Scholar). A reference induction factor was calculated for each gene by averaging the induction factors of each respective gene from 22 experiments (four independent experiments with wild-type cells and two independent experiments with each of the ΔHik33, ΔHik34, ΔHik16, ΔHik41, ΔHik10, ΔRre31, ΔRre1, ΔRre17, and ΔRre3 mutants) and used for evaluation of changes in the gene expression in order to avoid variations caused by experimental deviations. The effect of mutation of a Hik or a Rre on gene expression (RE: effective ratio) was evaluated quantitatively as shown in Equation 1. RE=(Induction Factor of a mutant sample−1.0)(Induction Factor of control sample−1.0)×100 Eq.1 In the equation, 1.0 was subtracted from each Induction Factor because the absence of a change in expression corresponds to an Induction Factor of 1.0. We assigned a salt-induced gene whose expression was reduced by mutation of a Hik or Rre when the RE was less than 50. Moreover, we identified a strictly regulated gene when the RE was less than 15. Under these conditions, the extent of induction was considered to be significantly reduced by inactivation of the respective Hik-Rre system. Slot-blot Screening of the Rre Mutant Library and DNA Microarray Analysis Identified Specific Sets of Salt Stress-inducible Genes under the Control of Rre31, Rre1, Rre17, and Rre3—In prokaryotic signal transduction pathways, a Hik is phosphorylated in response to a stimulus and then the phosphoryl group is transferred to the cognate Rre. After its phosphorylation, the Rre regulates the expression of specific genes (16Stock A.M. Robinson V.L. Goudreau P.N. Annu. Rev. Biochem. 2000; 69: 183-215Crossref PubMed Scopus (2398) Google Scholar). Although we demonstrated previously that salt stress due to 0.5 m NaCl is perceived by Hik33, Hik34, and a combination of Hik16 plus Hik41 (5Marin K. Suzuki I. Yamaguchi K. Ribbeck K. Yamamoto H. Kanesaki Y. Hagemann M. Murata N. Proc. Natl. Acad. Sci. U. S. A. 2003; 100: 9061-9066Crossref PubMed Scopus (136) Google Scholar), cognate response regulators of salt sensors have not yet been identified. Therefore, we attempted to identify candidates for Rres that might regulate salt stress-inducible gene expression. First, we screened a mutant library of Rres (www.kazusa.or.jp/cyanobase/Synechocystis/mutant) by RNA slot-blot hybridization. According to our previous results (5Marin K. Suzuki I. Yamaguchi K. Ribbeck K. Yamamoto H. Kanesaki Y. Hagemann M. Murata N. Proc. Natl. Acad. Sci. U. S. A. 2003; 100: 9061-9066Crossref PubMed Scopus (136) Google Scholar), we selected the following genes for use as probes: the slr1544 gene, which is regulated by salt stress under the control of Hik33; the dnaK2 gene, which is under the control of Hik34; and the slr0967 gene, which is under the control of Hik16 and Hik41. Fig. 1A shows some of the results of slot-blot hybridization. Among all the ΔRre mutant cells, only ΔRre31 cells demonstrated the absence of induction by salt stress of the slr1544 gene. In all the other ΔRre mutant cells, salt induction (induction by 0.5 m NaCl) was similar to that in wild-type cells. These observations suggested that Rre31 might be a candidate for the cognate Rre of Hik33 in the induction by salt stress of the expression of the slr1544 gene. When the dnaK2 gene was used as the probe, the absence of salt induction was evident only in ΔRre1 cells in our library of ΔRre mutants (Fig. 1B), suggesting that Rre1 might be a candidate for the cognate Rre of Hik34. We performed a similar experiment with slr0967 as the probe, and the results suggested that Rre17 might be a candidate for the cognate Rre of Hik16 and Hik41 (Fig. 1C). We examined the involvement of the Rre31, Rre1, and Rre17 in transduction of the salt-stress signal by monitoring salt-inducible gene expression using a DNA microarray. Moreover, we postulated that Rre3, which has been shown to be involved in hyperosmotic signal transduction (6Paithoonrangsarid K. Shoumskaya M.A. Kanesaki Y. Satoh S. Tabata S. Los D.A. Zinchenko V.V. Hayashi H. Tanticharoen M. Suzuki I. Murata N. J. Biol. Chem. 2004; 279: 53078-53086Abstract Full Text Full Text PDF PubMed Scopus (107) Google Scholar), might function as a transducer in the salt-signaling pathway. Therefore, we also examined the effects of mutation of Rre3 on the expression of salt stress-inducible genes. Table I lists all the salt stress-inducible genes with induction factors higher than 4.0 that were affected (or not) by mutation of Rre31, Rre1, Rre17, and Rre3. The first group of genes, whose induction was diminished in ΔRre31 cells, included the hliA, hliB, and hliC genes for high light-inducible proteins, the sigD gene for RNA polymerase σ factor, and seven other genes for proteins of known and unknown function.Table ISalt stress-inducible genes and effects of the inactivation of Rre31, Rre1, Rre17, and Rre3 on the induction of these genes Cells, grown under control conditions, were incubated with 0.5 m NaCl for 20 min. Each value indicates the ratio of the level of the transcript in salt-stressed cells to that in controls. The numbering of ORFs corresponds to that in the database on the Cyanobase website (ftp.kazusa.or.jp/pub/cyano/Synechocystis/6803ann_new_old3.xls). This table lists the salt stress-inducible genes with induction factors higher than 4.0 in control cells (average of values from 22 independent experiments; see “Experimental Procedures” for full explanation), and their categorization depends on values of RE lower than 50. The entire list can be accessed at www.genome.ad.jp/kegg/expression/.ORFNameProductInduction by 0.5 m NaClWTaThese values represent the averaged induction factors and ranges of deviation of results, which were calculated from the results of four independent experiments with wild-type cellsΔRre31bThese values represent the averaged induction factors and ranges of deviation of results, which were calculated from the results of two independent experiments with ΔRre mutant cellsΔRre1bThese values represent the averaged induction factors and ranges of deviation of results, which were calculated from the results of two independent experiments with ΔRre mutant cellsΔRre17bThese values represent the averaged induction factors and ranges of deviation of results, which were calculated from the results of two independent experiments with ΔRre mutant cellsΔRre3bThese values represent the averaged induction factors and ranges of deviation of results, which were calculated from the results of two independent experiments with ΔRre mutant cellsControlcInduction factors and S.D. of controls were calculated by averaging the induction factors from 22 independent experiments (four with wild-type cells and two each with ΔHik33, ΔHik34, ΔHik16, ΔHik41, ΔHik10, ΔRre31, ΔRre1, ΔRre17, and ΔRre3 mutant cells)Genes whose induction by salt stress was reduced in ΔRre31 cells (Group 1)slr1544dUnderlining of an ORF indicates a strictly regulated gene whose RE was lower than 15 for some ΔRrePutative protein23.2 ± 0.10.8 ± 2.4 (-1)eThe number in parentheses is the RE (effective ratio; for definition see “Experimental Procedures”)22.7 ± 5.4 (117)44.5 ± 0.9 (234)40.3 ± 3.7 (212)19.6 ± 3.3slr1687fThe slr1687 gene is categorized as a gene whose inducibility was reduced in ΔRre31 cells (RE = 24), but not in ΔRre1 (RE = 24) cells, because mutation of the cognate Hik33 and Hik34 yielded values of RE of 35 and 54, respectivelyPutative protein16.0 ± 0.43.5 ± 0.7 (24)3.4 ± 0.9 (24)21.1 ± 0.9 (195)19.0 ± 0.5 (174)11.3 ± 1.5ssr2595hliBHigh light-inducible protein15.1 ± 0.10.7 ± 3.4 (-3)15.8 ± 1.3 (151)19.5 ± 0.2 (189)14.4 ± 0.1 (137)10.8 ± 1.6ssl2542hliAHigh light-inducible protein9.8 ± 0.01.0 ± 2.2 (0)11.3 ± 4.0 (140)13.4 ± 2.3 (169)16.7 ± 0.6 (214)8.3 ± 1.3sll1722Putative protein10.3 ± 0.23.2 ± 6.0 (33)11.4 ± 0.0 (155)5.3 ± 0.1 (64)10.9 ± 2.9 (148)7.7 ± 1.2sll1621Membrane protein8.4 ± 0.83.2 ± 0.1 (36)5.6 ± 0.2 (74)8.8 ± 0.7 (127)8.9 ± 1.2 (128)7.1 ± 0.5ssr2016Putative protein6.4 ± 0.00.8 ± 0.8 (-4)16.6 ± 2.2 (255)17.0 ± 1.3 (262)12.0 ± 0.5 (179)7.1 ± 1.3ssl1633hliCHigh light-inducible protein4.9 ± 0.11.3 ± 0.3 (7)12.4 ± 0.7 (229)11.0 ± 0.4 (201)8.6 ± 1.4 (153)6.0 ± 0.9sll1483Periplasmic protein8.0 ± 0.00.8 ± 0.6 (-5)5.9 ± 0.2 (110)11.2 ± 2.9 (226)10.7 ± 1.6 (217)5.5 ± 0.9sll2012sigDRNA polymerase σ factor4.9 ± 0.41.8 ± 0.6 (21)5.6 ± 0.6 (126)6.8 ± 0.1 (157)6.8 ± 0.3 (158)4.7 ± 0.4sll1797ycf21Ycf21 gene product6.2 ± 0.22.0 ± 0.4 (30)5.1 ± 0.1 (122)6.0 ± 0.3 (148)6.2 ± 0.9 (155)4.4 ± 0.5Genes whose induction by salt stress was reduced in ΔRre1 cells (Group 2)sll0528Putative protein74.4 ± 4.013.6 ± 5.3 (27)1.5 ± 3.6 (1)74.6 ± 8.6 (160)106.9 ± 9.6 (230)47.1 ± 7.9sll1514hspASmall heat-shock protein49.7 ± 6.843.1 ± 1.6 (102)1.5 ± 0.3 (1)71.0 ± 1.1 (170)54.4 ± 6.4 (130)42.1 ± 5.1slr0959Putative protein19.3 ± 1.120.7 ± 0.2 (114)1.7 ± 0.7 (4)27.6 ± 3.8 (153)20.9 ± 2.8 (115)18.3 ± 2.1sll0306sigBRNA polymerase σ factor20.3 ± 2.218.5 ± 1.6 (118)2.7 ± 0.6 (11)16.1 ± 1.0 (101)26.2 ± 7.9 (170)15.9 ± 1.7slr1641clpB1ClpB protein22.3 ± 1.314.8 ± 0.6 (97)0.8 ± 0.3 (-2)20.2 ± 1.2 (135)25.4 ± 4.7 (172)15.2 ± 1.8slr1603Putative protein22.5 ± 2.114.8 ± 2.4 (103)1.0 ± 0.0 (0)13.4 ± 2.2 (93)22.1 ± 2.7 (157)14.4 ± 1.7slr0093dnaJHeat-shock protein 409.4 ± 2.017.1 ± 0.0 (138)0.9 ± 0.7 (-1)21.3 ± 1.5 (174)14.3 ± 0.8 (114)12.7 ± 1.4sll0846Putative protein14.6 ± 1.16.9 ± 0.1 (59)0.9 ± 1.1 (-1)14.9 ± 4.1 (138)17.7 ± 2.9 (165)11.1 ± 1.5ssl3044Hydrogenase component14.5 ± 0.06.0 ± 0.2 (51)2.6 ± 1.5 (16)17.9 ± 0.2 (171)14.1 ± 0.3 (133)10.9 ± 1.2slr1915Putative protein10.3 ± 0.514.0 ± 0.1 (143)0.7 ± 1.1 (-3)14.1 ± 1.3 (144)11.9 ± 0.0 (12110.0 ± 0.9slr1516sodBSuperoxide dismutase16.1 ± 2.08.9 ± 0.1 (90)1.9 ± 0.5 (10)11.6 ± 1.4 (120)12.5 ± 0.3 (131)9.8 ± 1.1sll0170dnaK2Heat-shock protein 7012.0 ± 0.28.4 ± 0.2 (96)1.0 ± 0.4 (1)12.1 ± 2.0 (143)14.1 ± 2.6 (170)8.7 ± 1.0sll1884Putative protein11.3 ± 0.87.7 ± 0.8 (91)1.0 ± 0.4 (0)9.4 ± 0.1 (114)11.6 ± 0.1 (144)8.3 ± 0.8slr1963Water-soluble carotenoid protein14.2 ± 2.24.5 ± 0.1 (48)0.8 ± 0.6 (-3)6.4 ± 0.1 (75)10.4 ± 0.6 (128)8.3 ± 1.0ssr3188Putative protein9.4 ± 1.56.6 ± 0.2 (86)1.4 ± 1.4 (7)9.6 ± 0.8 (132)9.3 ± 0.6 (128)7.5 ± 0.6slr1686Putative protein7.3 ± 0.76.9 ± 0.1 (103)1.2 ± 0.5 (4)10.1 ± 1.3 (160)6.7 ± 0.5 (100)6.7 ± 0.7slr0852Putative protein5.9 ± 0.19.4 ± 0.2 (161)0.9 ± 0.6 (-2)7.4 ± 0.3 (122)6.9 ± 1.0 (113)6.2 ± 0.5sll1167pbpPenicillin-binding protein 411.1 ± 0.56.4 ± 0.0 (107)1.2 ± 0.3 (3)6.5 ± 0.7 (110)5.3 ± 1.2 (85)6.1 ± 0.9slr0095O-methyltransferase4.8 ± 0.310.9 ± 0.3 (209)0.8 ± 0.5 (-5)8.3 ± 0.2 (155)5.4 ± 0.9 (92)5.7 ± 0.7slr1916Esterase6.1 ± 0.17.1 ± 0.4 (134)0.8 ± 0.2 (-4)6.5 ± 0.8 (121)4.8 ± 0.1 (83)5.5 ± 0.6ssl2971Putative protein7.2 ± 0.65.4 ± 0.4 (103)1.2 ± 0.3 (4)6.7 ± 0.8 (134)6.6 ± 1.1 (131)5.2 ± 0.5slr0853rimIRibosomal-protein-alanine acetyltransferase4.5 ± 0.57.5 ± 0.0 (165)1.1 ± 1.4 (2)5.2 ± 0.1 (106)4.5 ± 0.9 (90)4.9 ± 0.5slr1192Zinc-containing alcohol dehydrogenase family5.1 ± 0.25.0 ± 0.1 (111)1.2 ± 0.4 (6)4.7 ± 0.3 (101)6.2 ± 1.3 (144)4.6 ± 0.3sll0416groEL260-kDa chaperonin 25.5 ± 0.84.5 ± 0.2 (103)0.6 ± 0.3 (-11)5 0 ± 0.1 (119)5.8 ± 0.5 (144)4.4 ± 0.4sll1107Putative protein5.0 ± 0.35.3 ± 0.2 (133)1.0 ± 0.5 (-1)4.4 ± 0.7 (103)5.4 ± 0.3 (136)4.2 ± 0.3Genes whose induction by salt stress was reduced in ΔRre17 cells (Group 3)sll0939Putative protein35.8 ± 3.139.2 ± 0.8 (177)14.1 ± 0.7 (60)1.2 ± 0.0 (1)31.2 ± 5.6 (140)22.6 ± 3.8slr1704Putative protein11.9 ± 3.421.6 ± 1.0 (97)22.6 ± 0.9 (102)4.5 ± 1.2 (16)29.6 ± 2.8 (135)22.2 ± 3.0slr0967Putative protein32.3 ± 8.917.3 ± 1.2 (91)15.4 ± 0.5 (81)1.9 ± 0.1 (5)30.3 ± 1.6 (164)18.8 ± 2.9ssr2194Putative protein8.9 ± 2.114.5 ± 9.1 (91)18.1 ± 7.2 (115)4.8 ± 1.3 (25)15.7 ± 0.8 (99)15.9 ± 2.5sll0938N-Succinyldiaminopimelate aminotransferase8.5 ± 4.119.3 ± 0.3 (295)5.5 ± 0.1 (73)1.1 ± 0.0 (1)6.2 ± 0.3 (84)7.2 ± 1.5Gene whose induction by salt stress was reduced in ΔRre3 cells (Group 4)slr1204htrASerine protease HtrA9.5 ± 0.88.0 ± 0.1 (144)5.8 ± 0.0 (82)6.0 ± 1.0 (102)1.0 ± 0.0 (0)5.9 ± 0.7Genes whose induction by salt stress was unaffected in ΔRre31, ΔRre1, ΔRre17, and ΔRre3 cells (Group 5)sll1862Putative protein152.4 ± 26.4121.7 ± 3.3 (80)142.4 ± 10.1 (93)211.4 ± 28.6 (139)228.3 ± 2.9 (150)152.7 ± 12.6sll1863Putative protein106.5 ± 8.3141.4 ± 4.1 (115)110.8 ± 11.1 (90)160.8 ± 2.5 (131)133.0 ± 18.3 (108)122.7 ± 8.1sll1566ggpSGlucosylglycerol-phosphate synthase13.2 ± 2.39.6 ± 1.7 (53)16.1 ± 0.8 (93)31.0 ± 3.8 (184)24.6 ± 5.6 (145)17.2 ± 1.7sll1085glpDGlycerol-3-phosphate dehydrogenase9.7 ± 0.88.3 ± 2.6 (70)11.6 ± 0.2 (102)18.6 ± 1.2 (169)14.8 ± 4.3 (133)11.4 ± 1.0slr0895Putative protein7.2 ± 1.111.5 ± 0.5 (16)45.9 ± 1.5 (76)9.1 ± 0.3 (126)6.0 ± 1.5 (79)7.4 ± 0.8sll1652Putative protein6.1 ± 0.713.1 ± 0.3 (191)5.3 ± 0.6 (68)8.6 ± 0.4 (121)5.7 ± 0.9 (74)7.3 ± 0.6sll1594ndhRTranscriptional regulator of ndhF3 operon9.7 ± 0.47.1 ± 1.2 (101)8.6 ± 0.8 (126)5.6 ± 0.4 (77)6.3 ± 0.6 (88)7.0 ± 0.5slr1738Putative protein6.5 ± 0.15.3 ± 0.8 (83)3.7 ± 0.5 (53)7.3 ± 1.0 (122)7.6 ± 1.3 (128)6.9 ± 1.0ssr2153Putative protein4.6 ± 3.58.3 ± 0.4 (123)7.4 ± 3.6 (108)4.1 ± 0.6 (52)4.5 ± 0.9 (59)6.2 ± 0.4slr1932Putative protein5.8 ± 0.25.3 ± 1.0 (91)5.1 ± 0.2 (86)5.8 ± 0.5 (101)4.7 ± 0.2 (79)5.7 ± 0.4sll1620Putative protein6.0 ± 0.45.8 ± 0.7 (111)3.3 ± 0.7 (53)6.4 ± 1.6 (124)3.8 ± 0.4 (64)5.4 ± 0.5sll1653menGProbable phylloquinone-biosynthetic methyltransferase5.1 ± 0.17.9 ± 0.5 (163)3.9 ± 0.5 (69)6.4 ± 0.2 (128)4.7 ± 0.0 (89)5.2 ± 0.4slr1894Putative protein4.9 ± 0.13.3 ± 0.2 (53)3.9 ± 0.0 (114)6.1 ± 0.8 (57)6.0 ± 0.2 (84)4.5 ± 0.5slr1501Putative protein5.2 ± 0.22.9 ± 0.7 (67)5.0 ± 0.0 (84)3.0 ± 0.3 (150)4.0 ± 0.4 (146)4.4 ± 0.3a These values represent the averaged induction factors and ranges of deviation of results, which were calculated from the results of four independent experiments with wild-type cellsb These values represent the averaged induction factors and ra" @default.
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• W2129335564 date "2005-06-01" @default.
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• W2129335564 title "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" @default.
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• W2129335564 doi "https://doi.org/10.1074/jbc.m412174200" @default.
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