Inactivation of a low temperature-induced RNA helicase in synechocystis sp. PCC 6803: Physiological and morphological consequences

Plant and Cell Physiology

Volumn 53, Issue 4, 2012, Pages 646-658

  Rosana, Albert Remus R ^a   Ventakesh, Meghana ^b   Chamot, Danuta ^a   Patterson Fortin, Laura M ^a,c   Tarassova, Oxana ^a   Espie, George S ^b   Owttrim, George W ^a  

^a UNIVERSITY OF ALBERTA   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

^c UNIVERSITY OF FLORIDA   (United States)

Author keywords

Carbon acquisition and photosynthesis; Cell morphology; Cold stress; crhR inactivation; RNA helicase; Synechocystis sp. PCC 6803

Indexed keywords

REACTIVE OXYGEN METABOLITE; RNA HELICASE;

ARTICLE; COLD; ENZYMOLOGY; METABOLISM; SYNECHOCYSTIS;

COLD TEMPERATURE; REACTIVE OXYGEN SPECIES; RNA HELICASES; SYNECHOCYSTIS;

SYNECHOCYSTIS SP.; SYNECHOCYSTIS SP. PCC 6803;

EID: 84859746541     PISSN: 00320781     EISSN: 14719053     Source Type: Journal    
DOI: 10.1093/pcp/pcs020     Document Type: Article

References (43)

1. Battchikova, N., Eisenhut, M. and Aro, E.M. (2011) CyanobacterialNDH-1 complexes: novel insights and remaining puzzles. Biochim.Biophys. Acta 1807: 935-944.
2. Barral, P.M., Sarkar, D., Su, Z.Z., Barber, G.N., DeSalle, R., Racaniello, V.R.et al. (2009) Functions of the cytoplasmic RNA sensors RIG-I andMDA-5: key regulators of innate immunity. Pharmacol. Ther. 124:219-234.
3. Bennett, A. and Bogorad, L. (1973) Complementary chromatic adaptationin a filamentous blue-green alga. J. Cell Biol. 58: 419-435.
4. Chamot, D., Colvin, K.R., Kujat-Choy, S.L. and Owttrim, G.W. (2005)RNA structural rearrangement via unwinding and annealing by thecyanobacterial RNA helicase, CrhR. J. Biol. Chem. 280: 2036-2044.
5. Chamot, D., Magee, W.C., Yu, E. and Owttrim, G.W. (1999) A coldshock-induced cyanobacterial RNA helicase. J. Bacteriol. 181:1728-1732.
6. Chamot, D. and Owttrim, G.W. (2000) Regulation of coldshock-induced RNA helicase gene expression in the cyanobacteriumAnabaena sp. strain PCC 7120. J. Bacteriol. 182: 1251-1256. (Pubitemid 30104400)
7. Charollais, J., Dreyfus, M. and Iost, I. (2004) CsdA, a cold-shock RNAhelicase from Escherichia coli, is involved in the biogenesis of 50Sribosomal subunit. Nucleic Acids Res. 32: 2751-2759. (Pubitemid 38885946)
8. Charollais, J., Pflieger, D., Vinh, J., Dreyfus, M. and Iost, I. (2003) TheDEAD-box RNA helicase SrmB is involved in the assembly of 50Sribosomal subunits in Escherichia coli. Mol. Microbiol. 48:1253-1265. (Pubitemid 36718220)
9. Cordin, O., Banroques, J., Tanner, N.K. and Linder, P. (2006) TheDEAD-box protein family of RNA helicases. Gene 367: 17-37. (Pubitemid 43286737)
10. El-Fahmawi, B. and Owttrim, G.W. (2003) Polar-biased localization ofthe cold stress-induced RNA helicase, CrhC, in the cyanobacteriumAnabaena sp. strain PCC 7120. Mol. Microbiol. 50: 1439-1448. (Pubitemid 37475872)
11. Ensminger, I., Busch, F. and Huner, N.P.A. (2006) Photostasis and coldacclimation: sensing low temperature through photosynthesis.Physiol. Plant. 126: 28-44.
12. Espie, G.S., Miller, A.G., Birch, D.G. and Canvin, D.T. (1988a)Simultaneous transport of CO2 and HCO3-by the cyanobacteriumSynechococcus UTEX 625. Plant Physiol. 87: 551-554.
13. Espie, G.S., Miller, A.G. and Canvin, D.T. (1988b) Characterization ofthe Na+requirement in cyanobacterial photosynthesis. PlantPhysiol. 88: 757-763.
14. Ewen-Campen, B., Schwager, E.E. and Extavour, C.G. (2010) Themolecular machinery of germ line specification. Mol. Reprod. Dev.77: 3-18.
15. Fairman-Williams, M.E., Guenther, U.P. and Jankowsky, E. (2010) SF1and SF2 helicases: family matters. Curr. Opin. Struct. Biol. 20: 313-324.
16. Floriano, B., Herrero, A. and Flores, E. (1992) Isolation of arginineauxotrophs, cloning by mutant complementation, and sequenceanalysis of the argC gene from the cyanobacterium Anabaenaspecies PCC 7120. Mol. Microbiol. 6: 2085-2094.
17. Hunger, K., Beckering, C.L., Wiegeshoff, F., Graumann, P.L. andMarahiel, M.A. (2006) Cold-induced putative DEAD box RNAhelicases CshA and CshB are essential for cold adaptation andinteract with cold shock protein B in Bacillus subtilis. J. Bacteriol.188: 240-248.
18. Jagessar, K.L. and Jain, C. (2010) Functional and molecular analysis ofEscherichia coli strains lacking multiple DEAD-box helicases. RNA16: 1386-1392.
19. Jankowsky, E. (2011) RNA helicases at work: binding and rearranging.Trends Biochem. Sci. 36: 19-29.
20. Jones, P.G., Mitta, M., Kim, Y., Jiang, W. and Inouye, M. (1996) Coldshock induces a major ribosomal-associated protein that unwindsdouble- stranded RNA in Escherichia coli. Proc. Natl Acad. Sci. USA93: 76-80. (Pubitemid 26038105)
21. Kujat, S.L. and Owttrim, G.W. (2000) Redox-regulated RNA helicaseexpression. Plant Physiol. 124: 703-714.
22. Li, H. and Sherman, L.A. (2002) Characterization of Synechocystis sp.strain PCC 6803 and deltanbl mutants under nitrogen-deficientconditions. Arch. Microbiol. 178: 256-266. (Pubitemid 35025066)
23. Linder, P. and Owttrim, G.W. (2009) Plant RNA helicases: linking aberrantand silencing RNA. Trends Plant Sci. 14: 344-352.
24. Miller, A.G., Espie, G.S. and Canvin, D.T. (1988) Active transport of CO2by the cyanobacterium Synechococcus UTEX 625: measurement bymass spectrometry. Plant Physiol. 86: 677-683.
25. Miskiewicz, E., Ivanov, A.G. and Huner, N.P.A. (2002) Stoichiometry ofthe photosynthetic apparatus and phycobilisome structure of thecyanobacterium Plectonema boryanum UTEX 485 are regulated byboth light and temperature. Plant Physiol. 130: 1414-1425. (Pubitemid 35352965)
26. Miskiewicz, E., Ivanov, A.G., Williams, J.P., Khan, M.U., Falk, S. andHuner, N.P. (2000) Photosynthetic acclimation of the filamentouscyanobacterium, Plectonema boryanum UTEX 485, to temperatureand light. Plant Cell Physiol. 41: 767-775. (Pubitemid 30454055)
27. Nogami, T. and Mizushima, S. (1983) Outer membrane porins areimportant in maintenance of the surface structure of Escherichiacoli cells. J. Bacteriol. 156: 402-408. (Pubitemid 13022791)
28. Ogawa, T. and Mi, H. (2007) Cyanobacterial NADPH dehydrogenasecomplexes. Photosynth. Res. 93: 69-77.
29. Owttrim, G.W. (2006) RNA helicases and abiotic stress. Nucleic AcidsRes. 34: 3220-3230.
30. Patterson-Fortin, L.M., Colvin, K.R. and Owttrim, G.W. (2006) ALexA-related protein regulates redox-sensitive expression of thecyanobacterial RNA helicase, crhR. Nucleic Acids Res. 34:3446-3454.
31. Patterson-Fortin, L.M. and Owttrim, G.W. (2008) A SynechocystisLexA- orthologue binds direct repeats in target genes. FEBS Lett.582: 2424-2430.
32. Peil, L., Virumae, K. and Remme, J. (2008) Ribosome assembly inEscherichia coli strains lacking the RNA helicase DeaD/CsdA orDbpA. FEBS J. 275: 3772-3782. (Pubitemid 351990942)
33. Porra, R.J., Thompson, W.A. and Kriedemann, P.E. (1989)Determination of accurate extinction coefficients and simultaneousequations for assaying chlorophylls a and b extracted with fourdifferent solvents: verification of the concentration of chlorophyllstandards by atomic absorption spectroscopy. Biochim. Biophys.Acta 975: 384-394.
34. Prentki, P. and Krisch, H.M. (1984) In vitro insertional mutagenesiswith a selectable DNA fragment. Gene 29: 303-313. (Pubitemid 14038235)
35. Price, G.D., Badger, M.R., Woodger, F.J. and Long, B.M. (2008) Advancesin understanding the cyanobacterial CO2-concentratingmechanism(CCM): functional components, Ci transporters, diversity, genetic regulation and prospects for engineering into plants.J. Exp. Bot. 59: 1441-1461. (Pubitemid 351786553)
36. Rocak, S. and Linder, P. (2004) DEAD-box proteins: the driving forcesbehind RNA metabolism. Nat. Rev. Mol. Cell Biol. 5: 232-241. (Pubitemid 38325804)
37. Santiago-Santos, M.C., Ponce-Noyola, T., Olvera-Ramírez, R., Ortega-López, J. and Cañizares-Villanueva, R.O. (2004) Extraction and purificationof phycocyanin from Calothrix sp. Proc. Biochem. 39:2047-2052.
38. Shivaji, S. and Prakash, J.S. (2010) How do bacteria sense and respondto low temperature? Arch. Microbiol. 192: 85-95.
39. So, A.K., John-McKay, M. and Espie, G.S. (2002) Characterization of amutant lacking carboxysomal carbonic anhydrase from the cyanobacteriumSynechocystis PCC6803. Planta 214: 456-467. (Pubitemid 36072670)
40. Suzuki, I., Los, D.A., Kanesaki, Y., Mikami, K. and Murata, N. (2000) Thepathway for perception and transduction of low-temperaturesignals in Synechocystis. EMBO J. 19: 1327-1334. (Pubitemid 30151028)
41. Trubetskoy, D., Proux, F., Allemand, F., Dreyfus, M. and Iost, I. (2009)SrmB, a DEAD-box helicase involved in Escherichia coli ribosomeassembly, is specifically targeted to 23S rRNA in vivo. Nucleic AcidsRes. 37: 6540-6549.
42. Yu, E. and Owttrim, G.W. (2000) Characterization of the coldstress-induced cyanobacterial DEAD-box protein CrhC as an RNAhelicase. Nucleic Acids Res. 28: 3926-3934.
43. Zhang, P., Battchikova, N., Jansen, T., Appel, J., Ogawa, T. and Aro, E.M.(2004) Expression and functional roles of the two distinct NDH-1complexes and the carbon acquisition complex NdhD3/NdhF3/CupA/Sll1735 in Synechocystis sp PCC 6803. Plant Cell 16:3326-3340. (Pubitemid 41096009)