Simultaneous inactivation of sigma factors B and D interferes with light acclimation of the cyanobacterium Synechocystis sp. strain PCC 6803

Journal of Bacteriology

Volumn 191, Issue 12, 2009, Pages 3992-4001

  Pollari, Maija ^a   Ruotsalainen, Virpi ^a   Rantamäki, Susanne ^a   Tyystjärvi, Esa ^a   Tyystjärvi, Taina ^a  

^a UNIVERSITY OF TURKU   (Finland)

Author keywords

[No Author keywords available]

Indexed keywords

RNA POLYMERASE; SIGMA FACTOR; BACTERIAL PROTEIN;

ARTICLE; BACTERIAL GENE; BACTERIAL STRAIN; CONTROLLED STUDY; CYANOBACTERIUM; ELECTRON TRANSPORT; FLUORESCENCE; GENE EXPRESSION REGULATION; GENE INACTIVATION; LIGHT ADAPTATION; LIGHT DAMAGE; LIGHT STRESS; NONHUMAN; PHOTOINHIBITION; PHOTOSYNTHESIS; PHOTOTROPHIC BACTERIUM; PHOTOTROPHY; PRIORITY JOURNAL; PSBA GENE; REAL TIME POLYMERASE CHAIN REACTION; SIGB GENE; SIGD GENE; SYNECHOCYSTIS; THERMOLUMINESCENCE; TRANSCRIPTION INITIATION; GENE SILENCING; GENETICS; GROWTH, DEVELOPMENT AND AGING; LIGHT; METABOLISM; PHYSIOLOGY; RADIATION EXPOSURE;

CYANOBACTERIA; SYNECHOCYSTIS SP.;

BACTERIAL PROTEINS; GENE EXPRESSION REGULATION, BACTERIAL; GENE SILENCING; LIGHT; PHOTOSYNTHESIS; SIGMA FACTOR; SYNECHOCYSTIS;

EID: 67549146967     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.00132-09     Document Type: Article

References (59)

1. Asayama, M., and S. Imamura. 2008. Stringent promoter recognition and autoregulation by the group 3 sigma-factor SigF in the cyanobacterium Synechocystis sp. strain PCC 6803. Nucleic Acids Res. 36:5297-5305.
2. Bhaya, D., N. Watanabe, T. Ogawa, and A. R. Grossman. 1999. The role of an alternative sigma factor in motility and pilus formation in the cyanobacterium Synechocystis sp. strain PCC 6803. Proc. Natl. Acad. Sci. USA 96:3188-3193.
3. Bryant, D. A. 2003. The beauty in small things revealed. Proc. Natl. Acad. Sci. USA 100:9647-9649.
4. Burgess, R. R., A. A. Travers, J. J. Dunn, and E. K. F. Bautz. 1969. Factor stimulating transcription by RNA polymerase. Nature 221:43-46.
5. Constant, S., I. Perewoska, M. Alfonso, and D. Kirilovsky. 1997. Expression of the psbA gene during photoinhibition and recovery in Synechocystis PCC 6714: inhibition and damage of transcriptional and translational machinery prevent the restoration of photosystem II activity. Plant Mol. Biol. 34:1-13.
6. Dombroski, A. J., W. A. Walter, M. T. Record, D. A. Siegele, and C. A. Gross. 1992. Polypeptides containing highly conserved regions of transcription initiation factor sigma-70 exhibit specificity of binding to promoter DNA. Cell 70:501-512.
7. Field, C. B., M. J. Behrenfeld, J. T. Randerson, and P. Falkowski. 1998. Primary production of the biosphere: integrating terrestrial and oceanic components. Science 281:237-240. (Pubitemid 28334501)
8. Foyer, C. H., and G. Noctor. 2000. Oxygen processing in photosynthesis: regulation and signalling. New Phytol. 146:359-388. (Pubitemid 30441909)
9. Gill, R. T., E. Katsoulakis, W. Schmitt, G. Taroncher-Oldenburg, J. Misra, and G. Stephanopoulos. 2002. Genome-wide dynamic transcriptional profiling of the light-to-dark transition in Synechocystis sp. strain PCC 6803. J. Bacteriol. 184:3671-3681.
10. Havaux, M., G. Guedeney, M. Hagemann, N. Yeremenko, H. C. P. Matthijs, and R. Jeanjean. 2005. The chlorophyll-binding protein IsiA is inducible by high light and protects the cyanobacterium Synechocystis PCC6803 from photooxidative stress. FEBS Lett. 579:2289-2293.
11. Herranen, M., E.-M. Aro, and T. Tyystjärvi. 1999. Two distinct mechanisms regulate the transcription of photosystem II genes in Synechocystis sp. PCC 6803. Physiol. Plant. 112:531-539.
12. Hihara, Y. 1999. The molecular mechanism for acclimation to high light in cyanobacteria. Curr. Top. Plant Biol. 1:37-50.
13. Hihara, Y., A. Kamei, M. Kanehisa, A. Kaplan, and M. Ikeuchi. 2001. DNA microarray analysis of cyanobacterial gene expression during acclimation to high light. Plant Cell 13:793-806. (Pubitemid 32375902)
14. Huang, L., M. P. McCluskey, H. Ni, and R. A. LaRossa. 2002. Global gene expression profiles of the cyanobacterium Synechocystis sp. strain PCC6803 in response to irradiation with UV-B and white light. J. Bacteriol. 184:6845-6858.
15. Huckauf, J., C. Nomura, K. Forchhammer, and M. Hagemann. 2000. Stress responses of Synechocystis sp. strain PCC 6803 mutants impaired in genes encoding putative alternative sigma factors. Microbiology 146:2877-2889.
16. Ikeuchi, M., and S. Tabata. 2001. Synechocystis sp. PCC 6803: a useful tool in the study of genetics in cyanobacteria. Photosynth. Res. 70:73-83.
17. Imamura, S., M. Asayama, H. Takahashi, K. Tanaka, H. Takahashi, and M. Shirai. 2003. Antagonistic dark/light-induced SigB/SigD, group 2 sigma factors, expression through redox potential and their roles in cyanobacteria. FEBS Lett. 554:357-362. (Pubitemid 37412514)
18. Imamura, S., S. Yoshihara, S. Nakano, N. Shiozaki, A. Yamada, K. Tanaka, H. Takahashi, M. Asayama, and M. Shirai. 2003. Purification, characterization, and gene expression of all sigma factors of RNA polymerase in a cyanobacterium. J. Mol. Biol. 325:857-872.
19. Joshua, S., and C. W. Mullineaux. 2004. Phycobilisome diffusion is required for light-state transitions in cyanobacteria. Plant Physiol. 135:2112-2119. (Pubitemid 39182791)
20. Kaneko, T., S. Sato, H. Kotani, A. Tanaka, E. Asamizu, Y. Nakamura, N. Miyajima, M. Hirosawa, M. Sugiura, S. Sasamoto, T. Kimura, T. Hosouchi, A. Matsuno, A. Muraki, N. Nakazaki, K. Naruo, S. Okumura, S. Shimpo, C Takeuchi, T. Wada, A. Watanabe, M. Yamada, M. Yasuda, and S. Tabata. 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. 3:109-136.
21. Kojima, K., M. Oshita, Y. Nanjo, K. Kasai, Y. Tozawa, H. Hayashi, and Y. Nishiyama. 2007. Oxidation of elongation factor G inhibits the synthesis of the D1 protein of photosystem II. Mol. Microbiol. 65:936-947.
22. Krieger-Liszkay, A. 2005. Singlet oxygen production in photosynthesis, J. Exp. Bot. 56:337-346. (Pubitemid 40263280)
23. Li, L., R. M. Alvey, R. P. Bezy, and D. M. Kehoe. 2008. Inverse transcriptional activities during complementary chromatic adaptation are controlled by the response regulator RcaC binding to red and green light-responsive promoters. Mol. Microbiol. 68:286-297.
24. Marin, K., M. Stirnberg, M. Eisenhut, R. Krämer, and M. Hagemann. 2006. Osmotic stress in Synechocystis sp. PSS 6803: low tolerance toward nonionic osmotic stress results from lacking activation of glucosylglycerol accumulation. Microbiology 152:2023-2030.
25. Mohamed, A., J. Eriksson, H. D. Osiewacz, and C. Jansson. 1993. Differential expression of the psbA genes in the cyanobacterium Synechocystis 6803. Mol. Gen. Genet. 238:161-168.
26. Mohamed, A., and C. Jansson. 1989. Influence of light on accumulation of photosynthesis-specific transcripts in the cyanobacterium Synechocystis sp. PCC 6803. Plant Mol. Biol. 13:693-700.
27. Muramatsu, M., and Y. Hihara. 2007. Coordinated high-light response of genes encoding subunits of photosystem I is achieved by AT-rich upstream sequences in the cyanobacterium Synechocystis sp. strain PCC 6803. J. Bacteriol. 189:2750-2758. (Pubitemid 46556057)
28. Murata, N., S. Takahashi, Y. Nishiyama, and S. I. Allakhverdiev. 2007. Photoinhibition of photosystem II under environmental stress. Biochim. Biophys. Acta 1767:1414-1421.
29. Nishiyama, Y., S. I. Allakhverdiev, and N. Murata. 2005. Inhibition of the repair of PSII by oxidative stress in cyanobacteria. Photosynth. Res. 84:1-7.
30. Nishiyama, Y., H. Yamamoto, S. I. Allakhverdiev, M. Inaba, A. Yokota, and N. Murata. 2001. Oxidative stress inhibits the repair of photodamage to the photosynthetic machinery. EMBO J. 20:5587-5594. (Pubitemid 33010036)
31. Osanai, T., M. Ikeuchi, and K. Tanaka. 2008. Group 2 sigma factors in cyanobacteria. Physiol. Plant 133:490-506. (Pubitemid 351841671)
32. Osanai, T., Y. Kanesaki, T. Nakano, H. Takahashi, M. Asayama, M. Shirai, M. Kanehisa, I. Suzuki, N. Murata, and K. Tanaka. 2005. Positive regulation of sugar catabolic pathways in the cyanobacterium Synechocystis sp. PCC 6803 by the group 2 σ factor SigE. J. Biol. Chem. 280:30653-30659.
33. Pollari, M., L. Gunnelius, I. Tuominen, V. Ruotsalainen, E. Tyystjärvi, T. Salminen, and T. Tyystjärvi. 2008. Characterization of single and double inactivation strains reveals new physiological roles for group 2 sigma factors of the cyanobacterium Synechocystis sp. PCC 6803. Plant Physiol. 147:1994-2005. (Pubitemid 352844238)
34. Ramakers, C. J., M. Ruijter, R. H. L. Deprez, and A. F. M. Moorman. 2003. Assumption-free analysis of quantitative real-time polymerase chain reaction (PCR) data. Neurosci. Lett. 339:62-66.
35. Sakurai, I., M. Hagio, Z. Gombos, T. Tyystjärvi, V. Paakkarinen, E.-M. Aro, and H. Wada. 2003. Requirement of phosphatidylglycerol for maintenance of photosynthetic machinery. Plant Physiol. 133:1376-1384. (Pubitemid 37458035)
36. Seki, A., M. Hanaoka, Y. Akimoto, S. Masuda, H. Iwasaki, and K. Tanaka. 2007. Induction of a group 2 σ factor, RPOD3 by high light and the underlying mechanism in Synechococcus elongatus PCC 7942. J. Biol. Chem. 282:36887-36894.
37. Sicora, C. I., S. E. Appleton, C. M. Brown, J. Chung, J. Chandler, A. M. Cockshutt, I. Vass, and D. A. Campbell. 2006. Cyanobacterial psbA families in Anabaena and Synechocystis encode trace, constitutive and UVB-induced D1 isoforms. Biochim. Biophys. Acta 1757:47-56.
38. Sicora, C. I., F. M. Ho, T. Salminen, S. Styring, and E.-M. Aro. 2009. Transcription of a "silent" cyanobacterial psbA gene is induced by microaerobic conditions. Biochim. Biophys. Acta 1787:105-112.
39. Silva, P., E. Thompson, S. Bailey, O. Kruse, C. W. Mullineaux, C. Robinson, N. H. Mann, and P. Nixon. 2003. FtsH is involved in the early stages of repair of photosystem II in Synechocystis sp. PCC 6803. Plant Cell 15:2152-2164.
40. Singh, A. K., T. C. Summerfield, H. Li, and L. A. Sherman. 2006. The heat shock response in the cyanobacterium Synechocystis sp. strain PCC 6803 and regulation of gene expression by HrcA and SigB. Arch. Microbiol. 186:273-286.
41. Stelljes, C., and F. Koenig. 2007. Specific binding of D1 protein degradation products to the psbAI promoter in Synechococcus sp. strain PCC 7942. J. Bacteriol. 189:1722-1726.
42. Summerfield, T. C., and L. A. Sherman. 2007. Role of sigma factors in controlling global gene expression in light/dark transitions in the cyanobacterium Synechocystis sp. strain PCC 6803. J. Bacteriol. 189:7829-7840.
43. Summerfield, T. C., J. Toepel, and L. A. Sherman. 2008. Low-oxygen induction of normally cryptic psbA genes is cyanobacteria. Biochemistry 47:12939-12941.
44. Tuominen, I., M. Pollari, E. Tyystjärvi, and T. Tyystjärvi. 2006. The SigB sigma factor mediates high-temperature responses in the cyanobacterium Synechocystis sp. PCC6803. FEBS Lett. 580:319-323.
45. Tuominen, I., M. Pollari, E. A. von Wobeser, E. Tyystjärvi, B. W. Ibelings, H. C. P. Matthijs, and T. Tyystjärvi. 2008. Sigma factor SigC is required for heat acclimation of the cyanobacterium Synechocystis sp. strain PCC 6803. FEBS Lett. 582:346-350.
46. Tuominen, I., E. Tyystjärvi, and T. Tyystjärvi. 2003. Expression of primary sigma factor (PSF) and PSF-like sigma factors in the cyanobacterium Synechocystis sp. PCC 6803. J. Bacteriol. 185:1116-1119.
47. Tyystjärvi, E. 2008. Photoinhibition of photosystem II and photodamage of the oxygen evolving manganese cluster. Coord. Chem. Rev. 252:361-376.
48. Tyystjärvi, E., and I. Vass. 2004. Light emission as a probe of charge separation and recombination in the photosynthetic apparatus: relation of prompt fluorescence to delayed light emission and thermoluminescence, p. 363-388. In G. C. Papageorgiou and Govindjee (ed.), Chlorophyll a fluorescence: a signature of photosynthesis. Kluwer Academic Publishers, Dordrecht, The Netherlands.
49. Tyystjärvi, E., S. Rantamäki, and J. Tyystjärvi. Connectivity of photosystem II is the physical basis of retrapping in photosynthetic thermoluminescence. Biophys. J., in press.
50. Tyystjärvi, T., E.-M. Aro, C. Jansson, and P. Mäenpää . 1994. Changes of amino acid sequence in PEST-like area and QEEET motif affect degradation rate of D1 polypeptide in photosystem II. Plant Mol. Biol. 25:517-526.
51. Tyystjärvi, T., M. Herranen, and E.-M. Aro. 2001. Regulation of translation elongation in cyanobacteria: membrane targeting of the ribosome nascentchain complexes controls the synthesis of D1 protein. Mol. Microbiol. 40: 476-484.
52. Tyystjärvi, T., P. Mulo, P. Mäenpää, and E.-M. Aro. 1996. D1 polypeptide degradation may regulate psbA gene expression at transcriptional and translational levels in Synechocystis sp. PCC6803. Photosynth. Res. 47:111-120.
53. Tyystjärvi, T., I. Tuominen, M. Herranen, E.-M. Aro, and E. Tyystjärvi. 2002. Action spectrum of psbA transcription is similar to that of photoinhibition in Synechocystis sp. PCC 6803. FEBS Lett. 516:167-171.
54. Tyystjärvi, T., E. Tyystjärvi, I. Ohad, and E.-M. Aro. 1998. Exposure of Synechocystis 6803 cells to series of single turnover flashes increase the psbA transcript level by activating transcription and down-regulating psbA mRNA degradation. FEBS Lett. 436:483-487. (Pubitemid 28482986)
55. van Thor, J. J., C. W. Mullineaux, H. C. P. Matthijs, and K. J. Hellingwerf. 1998. Light Harvesting and state transitions in cyanobacteria. Bot. Acta 111:430-443. (Pubitemid 29043048)
56. Williams, J. K. G. 1988. Construction of specific mutations in photosystem II photosynthetic reaction center by genetic engineering methods in Synechocystis 6803. Methods Enzymol. 167:766-778.
57. Wilson, A., G. Ajlani, J. Z. Verbavatz, I. Vass, C. A. Kerfeld, and D. Kirilovsky. 2006. A soluble carotenoid protein involved in phycobilisome-related energy dissipation in cyanobacteria. Plant Cell 18:992-1007. (Pubitemid 43956149)
58. Wilson, A., C. Punginelli, A. Gall, C. Bonettit, M. Alexandre, J. M. Routaboul, C. A. Kerfeld, R. van Grondelle, B. Robert, J. T. M. Kennis, and D. Kirilovsky. 2008. A photoactive carotenoid protein acting as light intensity sensor. Proc. Natl. Acad. Sci. USA 105:12075-12080.
59. Yeremenko, N., R. Kouril, J. A. Ihalainen, S. D'Haene, N. van Oosterwijk, E. G. Andrizhiyevskaya, W. Keegstra, H. L. Dekker, M. Hagemann, E. J. Boekema, H. C. P. Matthijs, and J. P. Dekker. 2004. Supramolecular organization and dual function of the IsiA chlorophyll-binding protein in cyanobacteria. Biochemistry 43:10308-10313. (Pubitemid 39079304)