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

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 genes might and the specific Rre associated with each Hik to be is that Hiks might be involved in the sensing of salt stress that have not been because of of the the genome to salt stress. The responses of the genome be by DNA microarray A of the of each gene to in specific Hiks to the Hik that is associated with each gene and to genes that are not to Hiks that have been identified and be by In the present study, we identified and as possibly as well as the cognate Rres of Hik33, Hik34, Hik16, and We compared genes with hyperosmotic genes and found that the two kinds of stress induced the expression of genes to different extents. Our that the systems for of salt stress and hyperosmotic stress are but the two kinds of stress are perceived as different signals. and sp. PCC a was provided by J. G. K. I. and a was from S. of two as for of the gene knock-out libraries of Hiks and as (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, I. Los D.A. Kanesaki Y. Mikami K. Murata N. J. 2000; PubMed Scopus Google Scholar; see also cells were at in of with from at with by that as H. Murata N. Plant Physiol. 1989; Scopus Google Scholar). cells were the same as cells in the of in which was with an or for cells in which the genome been by of a gene or a gene of cells to salt stress, a of m NaCl was to of a of cells that been for to a of 0.5 The of salt stress was the same and used for the with hyperosmotic stress. of of were with an volume of that for of cells and to of of the cells by at for min at RNA was by the as I. Los D.A. J. Mol. Microbiol. 2000; 3: Scholar). The RNA was with to DNA and with a of and and in RNA and RNA slot-blot hybridization J. T. a Scholar), 10 of RNA were to a The RNA the was to with a specific that been from a salt stress-inducible such as or of RNA were by a that m The RNA was transferred to a by transfer and to with a specific and were as in with the and system with DNA were with hybridization and were in and signals from were with a were also with the gene for as a DNA DNA were from and genome-wide analysis of gene expression was as (3Kanesaki Y. Suzuki I. Allakhverdiev S.I. Mikami K. Murata N. Biochem. Biophys. Res. Commun. 2002; 290: 339-348Crossref PubMed Scopus (242) Google Scholar, I. Kanesaki Y. Mikami K. Kanehisa M. Murata N. Mol. Microbiol. 2001; 40: 235-244Crossref PubMed Scopus (197) Google Scholar). were with which included of the genes the Synechocystis were with the program in the of of genes to the of were by to the of signals from genes with the of genes for The expression of genes in cells salt stress was in The expression of genes in Hik cells was in two of induction factors and the of salt stress-inducible genes were as (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 induction was for each gene by the induction factors of each respective gene from with cells and two with each of the and and used for of changes in the gene expression in to by The of of a Hik or a Rre gene expression effective was as in of a of control In the was from each because the of a in expression to an of We a gene expression was by of a Hik or Rre when the was Moreover, we identified a regulated gene when the was these the of induction was to be by of the respective Hik-Rre of the Rre and DNA of the of Rre1, and signal transduction a Hik is in response to a and the group is transferred to the cognate the Rre the expression of specific genes Biochem. 2000; PubMed Scopus Google Scholar). Although we demonstrated 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 have not been we to for Rres that might regulate salt stress-inducible gene we screened a library of Rres by RNA slot-blot to previous (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 the genes for as the which is regulated by salt stress the control of the which is the control of and the which is the control of Hik16 and some of the of slot-blot the only cells demonstrated the of induction by salt stress of the In the salt induction by 0.5 m was to that in observations that might be a for the cognate Rre of in the induction by salt stress of the expression of the the gene was used as the the of salt induction was only in cells in library of mutants that Rre1 might be a for the cognate Rre of We a with as the and the that might be a for the cognate Rre of Hik16 and Hik41 We the of the Rre1, and in transduction of the signal by gene expression using a DNA Moreover, we that which been 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 as a in the we also the of of the expression of salt stress-inducible genes. the salt stress-inducible genes with induction factors that were by of Rre1, and The first group of induction was in included the and genes for the gene for RNA and genes for of and stress-inducible genes and of the of Rre1, and the induction of these genes control were with 0.5 m NaCl for the of the of the in cells to that in The of to that in the the the salt stress-inducible genes with induction factors in control cells of from see for and of The be at by 0.5 m the induction factors and of of which were from the of with the induction factors and of of which were from the of two with the induction factors and of of which were from the of two with the induction factors and of of which were from the of two with the induction factors and of of which were from the of two with factors and of were by the induction factors from with cells and two each with and induction by salt stress was in cells of an a regulated gene was for some in is the for see gene is as a gene was in cells but not in because of the cognate and of of and 0.5 0.2 0.1 0.1 0.1 0.2 0.5 0.2 0.1 gene 0.1 induction by salt stress was in cells 0.2 0.1 0.2 0.2 0.1 0.1 0.5 0.2 0.1 0.1 0.1 0.1 0.2 0.1 0.5 0.5 0.2 0.5 0.2 0.2 0.1 0.1 0.1 0.2 0.1 0.5 0.2 0.5 induction by salt stress was in cells 0.5 0.1 0.1 induction by salt stress was in cells 0.1 induction by salt stress was in and cells 0.2 0.5 of 0.5 0.2 0.5 0.2 0.5 0.5 0.2 0.2 0.2 the induction factors and of of which were from the of with the induction factors and of of which were from the of two with factors and of were by the induction factors from with cells and two each with and of an a regulated gene was for some The in is the for see The gene is as a gene was in cells but not in because of the cognate and of of and in a The group of induction was in included the for a for for for for for RNA for and genes for of and A of group is that of the genes of which are involved in the and of Full Text Full Text PDF PubMed Scopus Google Scholar). The group of induction of expression was in included genes for an aspartate and for of The group of induction by salt stress was in was of the gene for a The induction of expression of a group of genes was by of of these Rres. group included the for for for a of of the and a of genes for of and The in that of salt stress-inducible genes with induction factors were the control of Rre1, and However, of the salt stress-inducible genes were regulated by as which might not an Rre as a DNA Hik33, Hik34, Hik16, and as of the of DNA we these to in the of in Hik33, Hik34, Hik16, and Hik41 as well as in Hik10, the cognate histidine of 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), salt stress-inducible gene We compared the of expression of salt stress-inducible genes in Hik cells with those in Rre The in that the expression of salt stress-inducible genes induction by salt stress was by was also by Hik33, with the of In the of the expression of salt stress-inducible genes the control of Rre1 was by of However, the of expression of several the and genes as well as that of some genes for of and was in cells but not in cells observations that there might be another Hik that salt stress and the signal to A was found in the of 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). Studies with a yeast two-hybrid system that might be the cognate Hik of Rre1 (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 be involved in salt In the of the salt stress-inducible genes expression was by the induction of gene expression was also by Hik16 and as in However, there are genes induction by salt stress was in cells but not in and DNA microarray analysis also that regulated the expression of the salt stress-inducible gene induction was by of the of Hik33, Hik34, Hik16, and the induction by salt stress of gene expression control were with 0.5 m NaCl for the of the of the in cells to that in The of to that in the the the salt stress-inducible genes with induction factors in control cells of from see for and of The be at by 0.5 m the induction factors and of of which were from the of with the induction factors and of of which were from the of two with the induction factors and of of which were from the of two with the induction factors and of of which were from the of two with the induction factors and of of which were from the of two with the induction factors and of of which were from the of two with factors and of were by the induction factors from with cells and two each with and induction by salt stress was in cells of a regulated gene was for some 0.1 in is the for see 0.1 0.5 0.2 salt stress-inducible expression of the gene was by but not by 0.1 0.2 0.5 0.1 0.2 0.5 gene 0.2 0.1 0.2 0.5 induction by salt stress was in cells 0.2 0.1 0.1 0.2 0.5 0.1 0.1 0.5 0.2 0.2 0.1 0.2 0.1 0.5 0.1 0.2 0.5 0.5 0.1 0.2 0.5 0.1 0.5 0.2 0.1 0.1 0.2 0.2 0.5 0.1 induction by salt stress was in 0.1 0.5 0.1 0.1 induction by salt stress was in cells 0.1 0.1 induction by salt stress was in and cells 0.2 0.5 of 0.1 0.1 0.5 0.2 0.2 0.2 0.1 0.5 0.5 0.1 0.2 0.2 0.2 0.2 the induction factors and of of which were from the of with the induction factors and of of which were from the of two with factors and of were by the induction factors from with cells and two each with and of a regulated gene was for some The in is the for see The salt stress-inducible expression of the gene was by but not by in a of the Rre expression of a of genes was by in the Rres We the Rre library by slot-blot hybridization using the and which to group of as Our that the expression of these genes was not in of the mutants not and that the expression of the genes in group might be regulated by some In sp. PCC a system of and the expression of genes in response to and stress N. J. 2002; PubMed Scopus Google Scholar). The of and in Synechocystis are N. J. 2002; PubMed Scopus Google Scholar) and by a we used DNA microarray analysis to the expression of genes in We found that of the gene not the expression of genes not observations suggest that not transfer the signal to of the of in Rres the of DNA microarray analysis that the expression of the gene was regulated by the Hik33-Rre31 We by the of and to the induction by salt stress of that the induction by salt stress of expression of the gene was in both and the group of genes by Hik34, we the gene to the of and Rre1 to salt induction by that the of induction of expression of the gene was in and We also the induction by salt stress of the gene in and cells by Our that the expression of was by of Hik16, or The of also demonstrated that the of induction by salt stress of the gene was in and Hik-Rre in the and of in of and libraries by RNA slot-blot hybridization and the genome-wide analysis of gene expression using DNA that the salt signal is perceived by histidine such as Hik33, Hik34, Hik16 plus and response such as Rre1, and salt signals from the Hiks and regulate the expression of a of genes. a of the salt systems of these Hiks and and it the genes that are by the systems. Rre1 seems to the signal from two is Hik34, and the is likely to be a Hik that a system with Although with yeast two-hybrid systems suggest that might with Rre1 (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), there is evidence for between these the of the Hik located of Rre1 an open In two systems, namely, and are involved in the transduction of or signals K. K. M. J. PubMed Google Scholar, K. J. PubMed Google Scholar, Microbiol. Mol. Biol. PubMed Google Scholar). cells a that of a histidine a and a response when cells are exposed to salt stress F. T. H. 1996; Full Text Full Text PDF PubMed Scopus Google Scholar, S. Microbiol. Mol. Biol. 2002; PubMed Scopus Google Scholar). In Synechocystis, we identified systems for the transduction of salt signals. Our were because we used Rre and Hik libraries in which of the Rres and Hiks been as well as genome-wide analysis of gene expression with the DNA analysis be to such as E. and it is likely that many systems be identified for the and transduction of salt signals. of Hik-Rre and but of Hik33-Rre31, or Hik10-Rre3, and systems to in the perception and transduction of both salt stress and 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). is as we demonstrated genes from hyperosmotic stress-inducible genes (3Kanesaki Y. Suzuki I. Allakhverdiev S.I. Mikami K. Murata N. Biochem. Biophys. Res. Commun. 2002; 290: 339-348Crossref PubMed Scopus (242) Google Scholar). we compared the sets of genes and hyperosmotic stress-inducible genes that were the control of Hik-Rre systems. Our to the in that in the of only the gene for was induced by both kinds of stress. In the of Hik16-Hik41-Rre17, only three namely, and were induced by both kinds of stress. are with the of Hik-Rre systems, in which a Hik and cognate Rre regulate the expression of one gene or a set of genes. The of genes the Synechocystis genome that and an and regulated and that the gene is located downstream of the the of seems likely that the expression of the and that of the gene are regulated in the of the three Hik-Rre systems, Hik33-Rre31, Hik34-Rre1, and each system regulated the expression of a group of genes that was induced by both kinds of stress and a group of genes expression was induced either by salt stress or by hyperosmotic stress. group of and some genes for of was by the Hik33-Rre31 the expression of these genes was induced by both salt stress and hyperosmotic stress. However, expression of another group that of the gene and was induced by hyperosmotic stress, but not by salt stress. In the of the or the expression of some such as and some genes for of and was induced by both salt stress and by hyperosmotic stress. Moreover, system regulated genes expression was specifically by salt stress, but not by hyperosmotic stress, such as the However, system also regulated genes expression was specifically by hyperosmotic stress, but not by salt stress, such as the Our that the systems, Hik33-Rre31 and or regulate the expression of distinct respective sets of genes different kinds of stress be by the of systems. might both salt stress and hyperosmotic stress and these signals to the not the expression of the two of genes the control of Hik33-Rre31 different of stress. The for the or systems is the expression of two of genes different of stress be seems to the of some that each system with that is to the specific of the stress. studies are to these factors and to how with the Hik-Rre systems. Hik-Rre systems are involved in perception and transduction of salt signals and hyperosmotic signals but regulate the expression of genes to different in of PDF