The importance of flavodoxin for environmental stress tolerance in photosynthetic microorganisms and transgenic plants. Mechanism, evolution and biotechnological potential

FEBS Letters

Volumn 586, Issue 18, 2012, Pages 2917-2924

  Lodeyro, Anabella F ^a   Ceccoli, Romina D ^a   Pierella Karlusich, Juan J ^a   Carrillo, Néstor ^a  

^a UNIVERSIDAD NACIONAL DE ROSARIO   (Argentina)

Author keywords

Ferredoxin; Flavodoxin; Oxido reductive process; Photosynthesis; Stress physiology

Indexed keywords

FERREDOXIN; FLAVODOXIN; IRON; REACTIVE OXYGEN METABOLITE; SULFUR;

ADAPTATION; AEROBIC METABOLISM; BIOTECHNOLOGY; CHLOROPLAST; CHLOROPLAST GENOME; CONFERENCE PAPER; CYANOBACTERIUM; ELECTRON TRANSPORT; ENVIRONMENTAL STRESS; EUKARYOTE; IRON DEFICIENCY; NONHUMAN; OXIDATION REDUCTION REACTION; PHOTOSYNTHESIS; PHOTOTROPHIC BACTERIUM; PLANT STRESS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INDUCTION; SIGNAL TRANSDUCTION; STARVATION; TRANSGENIC PLANT;

ALGAE; CYANOBACTERIA; EUKARYOTA;

EID: 84864935618     PISSN: 00145793     EISSN: 18733468     Source Type: Journal    
DOI: 10.1016/j.febslet.2012.07.026     Document Type: Review

References (95)

1. T. Hase, P. Schürmann, and D. Knaff The interaction of ferredoxin with ferredoxin-dependent enzymes J.H. Golbeck, Photosystem I: The Light-Driven Plastocyanin:Ferredoxin Oxidoreductase. Advances in Photosynthesis and Respiration 2006 Springer Dordrecht 477 498
2. + reductase catalytic mechanism Eur. J. Biochem. 270 2003 1900 1915
3. E.A. Ceccarelli, A.K. Arakaki, N. Cortez, and N. Carrillo Functional plasticity and catalytic efficiency in plant and bacterial ferredoxin-NADP(H) reductases Biochim. Biophys. Acta 1698 2004 155 165
4. M.D. Zurbriggen, V.B. Tognetti, M.F. Fillat, M.R. Hajirezaei, E.M. Valle, and N. Carrillo Combating stress with flavodoxin: a promising route for crop improvement Trend Biotechnol. 26 2008 531 537
5. + reductase Govindjee Photosynthesis: Photobiochemistry and Photobiophysics. Advances in Photosynthesis and Respiration 2001 Kluwer Academic Publishers Walnut Creek, California 605 634
6. G.T. Hanke, and T. Hase Variable photosynthetic roles of two leaf-type ferredoxins in Arabidopsis, as revealed by RNA interference Photochem. Photobiol. 84 2008 1302 1309
7. G.T. Hanke, Y. Kimata-Ariga, I. Taniguchi, and T. Hase A post genomic characterization of Arabidopsis ferredoxins Plant Physiol. 134 2004 255 264
8. Y. Kimata-Ariga Differential electron flow around photosystem I by two C(4)-photosynthetic-cell-specific ferredoxins EMBO J. 19 2000 5041 5050
9. H. Böhme, and B. Schrautemeier Comparative characterization of ferredoxins from heterocysts and vegetative cells of Anabaena variabilis Biochim. Biophys. Acta 891 1987 1 7
10. O. Vorst, F. van Dam, P. Weisbeek, and S. Smeekens Light-regulated expression of the Arabidopsis thaliana ferredoxin A gene involves both transcriptional and post-transcriptional processes Plant J. 3 1993 793 803
11. M.E. Petracek, L.F. Dickey, T.T. Nguyen, C. Gatz, D.A. Sowinski, G.C. Allen, and W.F. Thompson Ferredoxin-1 mRNA is destabilized by changes in photosynthetic electron transport Proc. Natl. Acad. Sci. USA 95 1998 9009 9013
12. V.B. Tognetti, M.D. Zurbriggen, E.N. Morandi, M.F. Fillat, E.M. Valle, M.R. Hajirezaei, and N. Carrillo Enhanced plant tolerance to iron starvation by functional substitution of chloroplast ferredoxin with a bacterial flavodoxin Proc. Natl. Acad. Sci. USA 104 2007 11495 11500
13. O. Thimm, B. Essigmann, S. Kloska, T. Altmann, and T.J. Buckhout Response of Arabidopsis to iron deficiency stress as revealed by microarray analysis Plant Physiol. 127 2001 1030 1043
14. P. Zimmermann, M. Hirsch-Hoffmann, L. Hennig, and W. Gruissem GENEVESTIGATOR. Arabidopsis microarray database and analysis toolbox Plant Physiol. 136 2004 2621 2632
15. V.B. Tognetti, J.F. Palatnik, M.F. Fillat, M. Melzer, M.R. Hajirezaei, E.M. Valle, and N. Carrillo Functional replacement of ferredoxin by a cyanobacterial flavodoxin in tobacco confers broad-range stress tolerance Plant Cell 18 2006 2035 2050
16. A.K. Singh, H. Li, and L.A. Sherman Microarray analysis and redox control of gene expression in the cyanobacterium Synechocystis sp. PCC 6803 Physiol. Plant. 120 2004 27 35
17. K. Mazouni, F. Domain, F. Chauvat, and C. Cassier-Chauvat Expression and regulation of the crucial plant-like ferredoxin of cyanobacteria Mol. Microbiol. 49 2003 1019 1029
18. R.D. Ceccoli, N.E. Blanco, M. Medina, and N. Carrillo Stress response of transgenic tobacco plants expressing a cyanobacterial ferredoxin in chloroplasts Plant Mol. Biol. 76 2011 535 544
19. M.F. Fillat, G. Sandmann, and C. Gómez-Moreno Flavodoxin from the nitrogen-fixing cyanobacterium Anabaena PCC7119 Arch. Microbiol. 150 1988 160 164
20. K.H. Dudley, A. Ehrenberg, P. Hemmerich, and F. Müller Spektren und Strukturen der am Flavin-Redoxsystem beteiligten Partikeln Helv. Chim. Acta 47 1964 1354 1383
21. + reductase. Role of flavodoxin residues in protein-protein interaction and electron transfer Biochemistry 44 2005 97 104
22. J. Sancho Flavodoxins: sequence, folding, binding, function and beyond Cell. Mol. Life Sci. 63 2006 855 864
23. M. Zheng, B. Doan, T.H. Scheider, and G. Storz OxyR and SoxRS regulation of fur J. Bacteriol. 181 1999 4639 4643
24. J. Freigang, K. Diederichs, K.P. Schafer, W. Welte, and R. Paul Crystal structure of oxidized flavodoxin, an essential protein in Helicobacter pylori Protein Sci. 11 2002 253 261
25. K.J. Puan, H. Wang, T. Dairi, T. Kuzuyama, and C.T. Morita FldA is an essential gene required in the 2-C-methyl-D-erythritol 4-phosphate pathway for isoprenoid biosynthesis FEBS Lett. 579 2005 3802 3806
26. + reductase J.H. Golbeck, Photosystem I: the Light-Driven Plastocyanin: Ferredoxin Oxidoreductase. Advances in Photosynthesis and Respiration 2006 Springer Dordrecht 455 476
27. H.P. Blaschkowski, G. Neuer, M. Ludwig-Festl, and J. Knappe Routes of flavodoxin and ferredoxin reduction in Escherichia coli. CoA-acylating pyruvate: flavodoxin and NADPH:flavodoxin oxidoreductases participating in the activation of pyruvate formate-lyase Eur. J. Biochem. 123 1982 563 569
28. P.J. Keeling, G. Burger, D.G. Durnford, B.F. Lang, R.W. Lee, R.E. Pearlman, A.J. Roger, and M.W. Gray The tree of eukaryotes Trends Ecol. Evol. 20 2005 670 676
29. + reductase system from Anabaena Biochimie 80 1998 837 846
30. C. Gómez-Moreno Protein engineering for the elucidation of the mechanism of electron transfer in redox proteins Biochem. Soc. Trans. 22 1994 796 800
31. +) reductase Biochim. Biophys. Acta 1787 2009 144 154
32. + reductase Proteins 38 2000 301 309
33. + oxidoreductase: the role of carboxyl groups, electrostatic surface potential, and molecular dipole moment Protein Sci. 2 1993 1126 1135
34. J.A. Imlay Iron-sulphur clusters and the problem with oxygen Mol. Microbiol. 59 2006 1073 1082
35. G. Wächtershäuser Groundworks for an evolutionary biochemistry: the iron-sulphur world Prog. Biophys. Mol. Biol. 58 1992 85 201
36. G. Wächtershäuser On the chemistry and evolution of the pioneer organism Chem. Biodivers. 4 2007 584 602
37. C.J. Bjerrum, and D.E. Canfield Ocean productivity before about 1.9 Gyr ago limited by phosphorus adsorption onto iron oxides Nature 417 2002 159 162
38. R. Mittler, S. Vanderauwera, M. Gollery, and F. van Breusegem Reactive oxygen gene network of plants Trends Plant Sci. 9 2004 490 498
39. S. Holtgrefe, K.P. Bader, P. Horton, R. Scheibe, A. von Schaewen, and J.E. Backhausen Decreased content of leaf ferredoxin changes electron distribution and limits photosynthesis in transgenic potato plants Plant Physiol. 133 2003 1768 1778
40. I. Voss, M. Koelmann, J. Wojtera, S. Holtgrefe, C. Kitzmann, J.E. Backhausen, and R. Scheibe Knockout of major leaf ferredoxin reveals new redox-regulatory adaptations in Arabidopsis thaliana Physiol. Plant. 133 2008 584 598
41. N.E. Blanco Cyanobacterial flavodoxin complements ferredoxin deficiency in knocked-down transgenic tobacco plants Plant J. 65 2011 922 935
42. I. Nogués Role of the C-terminal tyrosine of ferredoxin- nicotinamide adenine dinucleotide phosphate reductase in the electron transfer processes with its protein partners ferredoxin and flavodoxin Biochemistry 43 2004 6127 6137
43. B. Palenik The tiny eukaryote Ostreococcus provides genomic insights into the paradox of plankton speciation Proc. Natl. Acad. Sci. USA 104 2007 7705 7710
44. K. Fukuyama, S. Wakabayashi, H. Matsubara, and L.J. Rogers Tertiary structure of oxidized flavodoxin from an eukaryotic red alga Chondrus crispus at 2.35-Å resolution. Localization of charged residues and implication for interaction with electron transfer partners J. Biol. Chem. 265 1990 15804 15812
45. M.D. Zurbriggen, V.B. Tognetti, and N. Carrillo Stress-inducible flavodoxin from photosynthetic microorganisms. The mystery of flavodoxin loss from the plant genome IUBMB Life 59 2007 355 360
46. D.L. Erdner, N.M. Price, G.J. Doucette, M.L. Peleato, and D.M. Anderson Characterization of ferredoxin and flavodoxin as markers of iron limitation in marine phytoplankton Mar. Ecol. Prog. Ser. 184 1999 43 53
47. Arabidopsis Genome Initiative Analysis of the genome sequence of the flowering plant Arabidopsis thaliana Nature 408 2000 796 815
48. S.A. Goff A draft sequence of the rice genome (Oryza sativa L. ssp. japonica) Science 296 2002 92 100
49. S.A. Rensing The Physcomitrella genome reveals evolutionary insights into the conquest of land by plants Science 319 2008 64 69
50. A.R. Krapp, R.E. Rodríguez, H.O. Poli, D.H. Paladini, J.F. Palatnik, and N. Carrillo The flavoenzyme ferredoxin (flavodoxin)-NADP(H) reductase modulates NADP(H) homeostasis during the soxRS response of Escherichia coli J. Bacteriol. 184 2002 1474 1480
51. B. Palenik Genome sequence of Synechococcus CC9311: insights into adaptation to a coastal environment Proc. Natl. Acad. Sci. USA 103 2006 13555 13559
52. T.D. Jickells Global iron connections between desert dust, ocean biogeochemistry, and climate Science 308 2005 67 71
53. W.G. Sunda, and S.A. Huntsman Iron uptake and growth limitation in oceanic and coastal phytoplankton Mar. Chem. 50 1995 189 206
54. W.G. Sunda, D. Swift, and S.A. Huntsman Iron content of oceanic marine phytoplankton Nature 351 1991 55 57
55. S.W. Chisholm Phytoplankton size P.G. Falkowski, A.D. Woodhead, Primary Productivity and Biogeochemical Cycles in the Sea 1992 Plenum Press New York 213 237
56. E. Toulza, A. Tagliabue, S. Blain, and G. Piganeau Analysis of the global ocean sampling (GOS) project for trends in iron uptake by surface ocean microbes PLoS One 7 2012 e30931
57. R.F. Strzepek, and P.J. Harrison Photosynthetic architecture differs in coastal and oceanic diatoms Nature 431 2004 689 692
58. A.E. Allen Whole-cell response of the pennate diatom Phaeodactylum tricornutum to iron starvation Proc. Natl. Acad. Sci. USA 105 2008 10438 10443
59. M.L. Cuvelier Targeted metagenomics and ecology of globally important uncultured eukaryotic phytoplankton Proc. Natl. Acad. Sci. USA 107 2010 14679 14684
60. B. Palenik The genome of a motile marine Synechococcus Nature 424 2003 1037 1042
61. 6: Ferredoxin/Flavodoxin Reductase 2006 Springer Dordrecht 683 696
62. G. Rocap Genome divergence in two Prochlorococcus ecotypes reflects oceanic niche differentiation Nature 424 2003 1042 1047
63. T.S. Bibby, Y. Zhang, and M. Chen Biogeography of photosynthetic light-harvesting genes in marine phytoplankton PLoS One 4 2009 e4601
64. L.P. Whitney, J.J. Lins, M.P. Hughes, M.L. Wells, P.D. Chappell, and B.D. Jenkins Characterization of putative iron responsive genes as species-specific indicators of iron stress in thalassiosiroid diatoms Front. Microbiol. 2 2011 e234
65. M.L. Guerinot, and Y. Yi Iron: nutritious, noxious, and not readily available Plant Physiol. 104 1994 815 820
66. H.V. Scheller In vitro cyclic electron transport in barley thylakoids follows two independent pathways Plant Physiol. 110 1996 187 194
67. A. Zöllner, I. Nogués, A. Heinz, M. Medina, C. Gómez-Moreno, and R. Bernhardt Analysis of the interaction of a hybrid system consisting of bovine adrenodoxin reductase and flavodoxin from the cyanobacterium Anabaena PCC 7119 Bioelectrochemistry 63 2004 61 65
68. T. Coba de la Peña, F.J. Redondo, E. Manrique, M.M. Lucas, and J.J. Pueyo Nitrogen fixation persists under conditions of salt stress in transgenic Medicago truncatula plants expressing a cyanobacterial flavodoxin Plant Biotechnol. J. 8 2010 1 12
69. Ceccoli, R.D. et al. (2012) Flavodoxin displays dose-dependent effects on photosynthesis and stress tolerance when expressed in transgenic tobacco plants. Planta, in press. DOI 10.1007/s00425-012-1695-x.
70. M.D. Zurbriggen, N. Carrillo, V.B. Tognetti, M. Melzer, M. Peisker, B. Hause, and M.R. Hajirezaei Chloroplast-generated reactive oxygen species play a major role in localized cell death during the non-host interaction between tobacco and Xanthomonas campestris pv. vesicatoria Plant J. 60 2009 962 973
71. F.J. Redondo, T. Coba de la Peña, C.N. Morcillo, M.M. Lucas, and J.J. Pueyo Overexpression of flavodoxin in bacteroids induces changes in antioxidant metabolism leading to delayed senescence and starch accumulation in alfalfa root nodules Plant Physiol. 149 2009 1166 1178
72. A. Shvaleva, T. Coba de la Peña, A. Rincón, C.N. Morcillo, V.S. García de la Torre, M.M. Lucas, and J.J. Pueyo Flavodoxin overexpression reduces cadmium-induced damage in alfalfa root nodules Plant Soil 326 2010 109 121
73. R. Scheibe Malate valves to balance cellular energy supply Physiol. Plant. 120 2004 21 26
74. K.K. Niyogi Safety valves for photosynthesis Curr. Opin. Plant Biol. 3 2000 455 460
75. J.P. Benz, M. Lintala, J. Soll, P. Mulo, and B. Bolter A new concept for ferredoxin-NADP(H) oxidoreductase binding to plant thylakoids Trends Plant Sci. 15 2010 608 613
76. R.E. Rodríguez Transgenic tobacco plants overexpressing chloroplastic ferredoxin-NADP(H) reductase display normal rates of photosynthesis and increased tolerance to oxidative stress Plant Physiol. 143 2007 639 649
77. M.F. Fillat, E. Flores, and C. Gómez-Moreno Homology of the N-terminal domain of the petH gene product from Anabaena sp. PCC 7119 to the CpcD phycobilisome linker polypeptide Plant Mol. Biol. 22 1993 725 729
78. + reductase Biochim. Biophys. Acta 1297 1996 200 206
79. + reductase confers increased tolerance to oxidative stress in plants FEBS Open Bio. 1 2011 7 13
80. V.J. Thannickal Oxygen in the evolution of complex life and the price we pay Am. J. Respir. Cell Mol. Biol. 40 2009 507 510
81. 6 and plastocyanin has been driven by geochemical changes G.A. Peschek, C. Obinger, G. Renger, Bioenergetic Processes of Cyanobacteria. From Evolutionary Singularity to Ecological Diversity 2011 Springer Dordrecht 607 630
82. P. Sétif Ferredoxin and flavodoxin reduction by photosystem I Biochim. Biophys. Acta 1507 2001 161 179
83. G.T. Hanke, Y. Satomi, K. Shinmura, T. Takao, and T. Hase A screen for potential ferredoxin electron transfer partners uncovers new, redox dependent interactions Biochim. Biophys. Acta 1814 2011 366 374
84. H. Bothe, O. Schmitz, M.G. Yates, and W.E. Newton Nitrogen fixation and hydrogen metabolism in cyanobacteria Microbiol. Mol. Biol. Rev. 74 2010 529 551
85. D.J. Schultz, M.C. Suh, and J.B. Ohlrogge Stearoyl-acyl carrier protein and unusual acyl-acyl carrier protein desaturase activities are differentially influenced by ferredoxin Plant Physiol. 124 2000 681 692
86. C. Miyake, and K. Asada Ferredoxin-dependent photoreduction of the monodehydroascorbate radical in spinach thylakoids Plant Cell Physiol. 35 1994 539 549
87. T. Muramoto, N. Tsurui, M.J. Terry, A. Yokota, and T. Kohchi Expression and biochemical properties of a ferredoxin-dependent heme oxygenase required for phytochrome chromophore synthesis Plant Physiol. 130 2002 1958 1966
88. F.Y. Chiu, Y.R. Chen, and S.L. Tu Electrostatic interaction of phytochromobilin synthase and ferredoxin for biosynthesis of phytochrome chromophore J. Biol. Chem. 285 2010 5056 5065
89. N. Frankenberg, and J.C. Lagarias Phycocyanobilin:ferredoxin oxidoreductase of Anabaena sp. PCC 7120. Biochemical and spectroscopic characterization J. Biol. Chem. 278 2003 9219 9226
90. N. Frankenberg, K. Mukougawa, T. Kohchi, and J.C. Lagarias Functional genomic analysis of the HY2 family of ferredoxin-dependent bilin reductases from oxygenic photosynthetic organisms Plant Cell 13 2001 965 978
91. M. Iwai, K. Takizawa, R. Tokutsu, A. Okamuro, Y. Takahashi, and J. Minagawa Isolation of the elusive supercomplex that drives cyclic electron flow in photosynthesis Nature 464 2010 1210 1213
92. G. DalCorso A complex containing PGRL1 and PGR5 is involved in the switch between linear and cyclic electron flow in Arabidopsis Cell 132 2008 273 285
93. M.L. Peleato, S. Ayora, L.A. Inda, and C. Gómez-Moreno Isolation and characterization of two different flavodoxins from the eukaryote Chlorella fusca Biochem. J. 302 1994 807 811
94. M. Hagemann, R. Jeanjean, S. Fulda, M. Havaux, F. Joset, and N. Erdmann Flavodoxin accumulation contributes to enhanced cyclic electron flow around photosystem I in salt-stressed cells of Synechocystis sp. strain PCC 6803 Physiol. Plant. 105 1999 670 678
95. M.A. Saito Iron conservation by reduction of metalloenzyme inventories in the marine diazotroph Crocosphaera watsonii Proc. Natl. Acad. Sci. USA 108 2011 2184 2189