Flavodiiron protein Flv2/Flv4-related photoprotective mechanism dissipates excitation pressure of PSII in cooperation with phycobilisomes in cyanobacteria

Plant Physiology

Volumn 164, Issue 2, 2014, Pages 805-818

  Bersanini, Luca ^a   Battchikova, Natalia ^a   Jokel, Martina ^a   Rehman, Ateeq ^b   Vass, Imre ^b   Allahverdiyeva, Yagut ^a   Aro, Eva Mari ^a  

^a UNIVERSITY OF TURKU   (Finland)

^b INSTITUTE OF EXPERIMENTAL MEDICINE   (Hungary)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; CAROTENOID; CHLOROPHYLL; CHLOROPHYLL A; ORANGE CAROTENOID PROTEIN, SYNECHOCYSTIS; OXYGEN; PLASTOQUINONE; SINGLET OXYGEN;

ARTICLE; GENETICS; GROWTH, DEVELOPMENT AND AGING; IMMUNOBLOTTING; KINETICS; METABOLISM; MUTATION; OPERON; OXIDATION REDUCTION REACTION; PHENOTYPE; PHOTOCHEMISTRY; PHOTOSYSTEM II; PHYCOBILISOME; SPECTROFLUOROMETRY; SYNECHOCYSTIS;

BACTERIAL PROTEINS; CAROTENOIDS; CHLOROPHYLL; IMMUNOBLOTTING; KINETICS; MUTATION; OPERON; OXIDATION-REDUCTION; OXYGEN; PHENOTYPE; PHOTOCHEMICAL PROCESSES; PHOTOSYSTEM II PROTEIN COMPLEX; PHYCOBILISOMES; PLASTOQUINONE; SINGLET OXYGEN; SPECTROMETRY, FLUORESCENCE; SYNECHOCYSTIS;

EID: 84893496515     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.113.231969     Document Type: Article

References (71)

1. Adir N, Zer H, Shochat S, Ohad I (2003) Photoinhibition-a historical perspective. Photosynth Res 76: 343-370
2. Ajlani G, Vernotte C (1998) Construction and characterization of a phycobiliprotein-less mutant of Synechocystis sp. PCC 6803. Plant Mol Biol 37: 577-580
3. Allahverdiyeva Y, Ermakova M, Eisenhut M, Zhang P, Richaud P, Hagemann M, Cournac L, Aro EM (2011) Interplay between flavodiiron proteins and photorespiration in Synechocystis sp. PCC 6803. J Biol Chem 286: 24007-24014
4. Allahverdiyeva Y, Mustila H, Ermakova M, Bersanini L, Richaud P, Ajlani G, Battchikova N, Cournac L, Aro EM (2013) Flavodiiron proteins Flv1 and Flv3 enable cyanobacterial growth and photosynthesis under fluctuating light. Proc Natl Acad Sci USA 110: 4111-4116
5. Allen MM (1968) Simple conditions for growth of unicellular blue-green algae on plates. J Phycol 4: 1-4
6. Aro EM, Virgin I, Andersson B (1993) Photoinhibition of photosystem II. Inactivation, protein damage and turnover. Biochim Biophys Acta 1143: 113-134
7. Ashby MK, Mullineaux CW (1999) The role of ApcD and ApcF in energy transfer from phycobilisomes to PSI and PSII in a cyanobacterium. Photosynth Res 61: 169-179
8. Badger MR, Price GD (2003) CO2 concentrating mechanisms in cyanobacteria: molecular components, their diversity and evolution. J Exp Bot 54: 609-622
9. Bailey S, Grossman A (2008) Photoprotection in cyanobacteria: regulation of light harvesting. Photochem Photobiol 84: 1410-1420
10. Campbell D, Hurry V, Clarke AK, Gustafsson P, Oquist G (1998a) Chlorophyll fluorescence analysis of cyanobacterial photosynthesis and acclimation. Microbiol Mol Biol Rev 62: 667-683
11. Campbell D, Eriksson MJ, Oquist G, Gustafsson P, Clarke AK (1998b) The cyanobacterium Synechococcus resists UV-B by exchanging photosystem II reaction-center D1 proteins. Proc Natl Acad Sci USA 95: 364-369
12. Clarke AK, Hurry VM, Gustafsson P, Oquist G (1993) Two functionally distinct forms of the photosystem II reaction-center protein D1 in the cyanobacterium Synechococcus sp. PCC 7942. Proc Natl Acad Sci USA 90: 11985-11989
13. Cser K, Vass I (2007) Radiative and non-radiative charge recombination pathways in Photosystem II studied by thermoluminescence and chlorophyll fluorescence in the cyanobacterium Synechocystis 6803. Biochim Biophys Acta 1767: 233-243
14. Durrant JR, Giorgi LB, Barber J, Klug DR, Porter G (1990) Characterization of triplet-states in isolated photosystem II reaction centres-oxygen quenching as a mechanism for photodamage. Biochim Biophys Acta Bioenerg 1017: 167-175
15. Eisenhut M, Georg J, Klähn S, Sakurai I, Mustila H, Zhang P, Hess WR, Aro EM (2012) The antisense RNA As1_flv4 in the cyanobacterium Synechocystis sp. PCC 6803 prevents premature expression of the flv4-2 operon upon shift in inorganic carbon supply. J Biol Chem 287: 33153-33162
16. El Bissati K, Delphin E, Murata N, Etienne AL, Kirilovsky D (2000) Photosystem II fluorescence quenching in the cyanobacterium Synechocystis PCC 6803: involvement of two different mechanisms. Biochim Biophys Acta 1457: 229-242
17. Ermakova M, Battchikova N, Allahverdiyeva Y, Aro EM (2013) Novel heterocyst-specific flavodiiron proteins in Anabaena sp. PCC 7120. FEBS Lett 587: 82-87
18. Frank HA, Cogdell RJ (1993) Photochemistry and function of carotenoids in photosynthesis. In A Young, G Britton, eds, Carotenoids in Photosynthesis, Chapman and Hall, London, pp 252-326
19. Fuhrmann E, Gathmann S, Rupprecht E, Golecki J, Schneider D (2009) Thylakoid membrane reduction affects the photosystem stoichiometry in the cyanobacterium Synechocystis sp. PCC 6803. Plant Physiol 149: 735-744
20. Giordano M, Beardall J, Raven JA (2005) CO2 concentrating mechanisms in algae: mechanisms, environmental modulation, and evolution. Annu Rev Plant Biol 56: 99-131
21. Graan T, Ort DR (1986) Detection of oxygen-evolving photosystem II centers inactive in plastoquinone reduction. Biochim Biophys Acta Bioenerg 852: 320-330
22. Helman Y, Tchernov D, Reinhold L, Shibata M, Ogawa T, Schwarz R, Ohad I, Kaplan A (2003) Genes encoding A-type flavoproteins are essential for photoreduction of O2 in cyanobacteria. Curr Biol 13: 230-235
23. Hideg E, Barta C, Kálai T, Vass I, Hideg K, Asada K (2002) Detection of singlet oxygen and superoxide with fluorescent sensors in leaves under stress by photoinhibition or UV radiation. Plant Cell Physiol 43: 1154-1164
24. Hideg E, Spetea C, Vass I (1994) Singlet oxygen production in thylakoid membranes during photoinhibition as detected by EPR spectroscopy. Photosynth Res 39: 191-199
25. Hideg É, Ogawa K, Kálai T, Hideg K (2001) Singlet oxygen imaging in Arabidopsis thaliana leaves under photoinhibition by excess photosynthetically active radiation. Physiol Plant 112: 10-14
26. Hihara Y, Sonoike K, Kanehisa M, Ikeuchi M (2003) DNA microarray analysis of redox-responsive genes in the genome of the cyanobacterium Synechocystis sp. strain PCC 6803. J Bacteriol 185: 1719-1725
27. Horton P, Ruban AV, Walters RG (1996) Regulation of light harvesting in green plants. Annu Rev Plant Physiol Plant Mol Biol 47: 655-684
28. Jallet D, Gwizdala M, Kirilovsky D (2012) ApcD, ApcF and ApcE are not required for the orange carotenoid protein related phycobilisome fluorescence quenching in the cyanobacterium Synechocystis PCC 6803. Biochim Biophys Acta 1817: 1418-1427
29. Kaplan A, Reinhold L (1999) CO2-concentrating mechanisms in photosynthetic microorganisms. Annu Rev Plant Physiol Plant Mol Biol 50: 539-570
30. Kós PB, Deák Z, Cheregi O, Vass I (2008) Differential regulation of psbA and psbD gene expression, and the role of the different D1 protein copies in the cyanobacterium Thermosynechococcus elongatus BP-1. Biochim Biophys Acta 1777: 74-83
31. Krieger-Liszkay A (2005) Singlet oxygen production in photosynthesis. J Exp Bot 56: 337-346
32. Krieger-Liszkay A, Fufezan C, Trebst A (2008) Singlet oxygen production in photosystem II and related protection mechanism. Photosynth Res 98: 551-564
33. Krupa Z, Oquist G, Gustafsson P (1991) Photoinhibition of photosynthesis and growth responses at different light levels in psbA gene mutants of the cyanobacterium Synechococcus Plant Physiol 82: 1-8
34. Kulkarni RD, Golden SS (1995) Form II of D1 is important during transition from standard to high light intensity in Synechococcus sp. strain PCC 7942. Photosynth Res 46: 435-443
35. Lagarde D, Beuf L, Vermaas W (2000) Increased production of zeaxanthin and other pigments by application of genetic engineering techniques to Synechocystis sp. strain PCC 6803. Appl Environ Microbiol 66: 64-72
36. Macpherson AN, Telfer A, Truscott TG, Barber J (1993) Direct detection of singlet oxygen from isolated photosystem II reaction centres. Biochim Biophys Acta Bioenerg 1143: 301-309
37. Mi H, Endo T, Ogawa T, Asada K (1995) Thylakoid membrane-bound, NADPH-specific pyridine-nucleotide dehydrogenase complex mediates cyclic electron-transport in the cyanobacterium Synechocystis sp. PCC 6803. Plant Cell Physiol 36: 661-668
38. Mohamed A, Eriksson J, Osiewacz HD, Jansson C (1993) Differential expression of the psbA genes in the cyanobacterium Synechocystis 6803. Mol Gen Genet 238: 161-168
39. Müller P, Li XP, Niyogi KK (2001) Non-photochemical quenching. A response to excess light energy. Plant Physiol 125: 1558-1566
40. Mullineaux CW, Emlyn-Jones D (2005) State transitions: an example of acclimation to low-light stress. J Exp Bot 56: 389-393
41. Mulo P, Sicora C, Aro EM (2009) Cyanobacterial psbA gene family: optimization of oxygenic photosynthesis. Cell Mol Life Sci 66: 3697-3710
42. Nixon PJ, Barker M, Boehm M, de Vries R, Komenda J (2005) FtsHmediated repair of the photosystem II complex in response to light stress. J Exp Bot 56: 357-363
43. Prasil O, Adir N, Ohad I (1992) Dynamics of photosystem II: mechanism of photoinhibition and recovery process. In J Barber, ed, Topics in Photosynthesis, The Photosystems: Structure, Function and Molecular Biology, Elsevier, Amsterdam, pp 220-250
44. Price GD, Badger MR, Woodger FJ, Long BM (2008) Advances in understanding the cyanobacterial CO2-concentrating-mechanism (CCM): functional components, Ci transporters, diversity, genetic regulation and prospects for engineering into plants. J Exp Bot 59: 1441-1461
45. Ramakers C, Ruijter JM, Deprez RH, Moorman AF (2003) Assumptionfree analysis of quantitative real-time polymerase chain reaction (PCR) data. Neurosci Lett 339: 62-66
46. Rehman AU, Cser K, Sass L, Vass I (2013) Characterization of singlet oxygen production and its involvement in photodamage of photosystem II in the cyanobacterium Synechocystis PCC 6803 by histidine-mediated chemical trapping. Biochim Biophys Acta 1827: 689-698
47. Sander J, Nowaczyk M, Buchta J, Dau H, Vass I, Deák Z, Dorogi M, Iwai M, Rögner M (2010) Functional characterization and quantification of the alternative PsbA copies in Thermosynechococcus elongatus and their role in photoprotection. J Biol Chem 285: 29851-29856
48. Schreiber U, Endo T, Mi H, Asada K (1995) Quenching analysis of chlorophyll fluorescence by the saturation pulse method: particular aspects relating to the study of eukaryotic algae and cyanobacteria. Plant Cell Physiol 36: 873-882
49. Summerfield TC, Nagarajan S, Sherman LA (2011) Gene expression under low-oxygen conditions in the cyanobacterium Synechocystis sp. PCC 6803 demonstrates Hik31-dependent and-independent responses. Microbiology 157: 301-312
50. Svensson B, Vass I, Styring S (1991) Sequence analysis of the D1 and D2 reaction center proteins of photosystem II. Z Naturforsch C 46: 765-776
51. Takishita K, Uchida A (1999) Molecular cloning and nucleotide sequence analysis of psbA from the dinoflagellates: origin of the dinoflagellate plastid. Phycol Res. 47: 207-216
52. Telfer A, Bishop SM, Phillips D, Barber J (1994) Isolated photosynthetic reaction center of photosystem II as a sensitizer for the formation of singlet oxygen. Detection and quantum yield determination using a chemical trapping technique. J Biol Chem 269: 13244-13253
53. Thomas JC, Ughy B, Lagoutte B, Ajlani G (2006) A second isoform of the ferredoxin:NADP oxidoreductase generated by an in-frame initiation of translation. Proc Natl Acad Sci USA 103: 18368-18373
54. Tian L, van Stokkum IH, Koehorst RB, Jongerius A, Kirilovsky D, van Amerongen H (2011) Site, rate, and mechanism of photoprotective quenching in cyanobacteria. J Am Chem Soc 133: 18304-18311
55. Tichý M, Lupínková L, Sicora C, Vass I, Kuviková S, Prásil O, Komenda J (2003) Synechocystis 6803 mutants expressing distinct forms of the photosystem II D1 protein from Synechococcus 7942: relationship between the psbA coding region and sensitivity to visible and UV-B radiation. Biochim Biophys Acta 1605: 55-66
56. Trebst A (1980) Inhibitors in electron flow: tools for the functional and structural localization of carriers and energy conservation sites. Methods Enzymol 69: 675-715
57. Trebst A, Depka B, Holländer-Czytko H (2002) A specific role for tocopherol and of chemical singlet oxygen quenchers in the maintenance of photosystem II structure and function in Chlamydomonas reinhardtii. FEBS Lett 516: 156-160
58. Tyystjärvi E (2008) Photoinhibition of photosystem II and photodamage of the oxygen evolving manganese cluster. Coord Chem Rev 252: 361-376
59. van Thor JJ, Mullineaux CW, Matthijs HCP, Hellingwerf KJ (1998) Lightharvesting and state transitions in cyanobacteria. Bot Acta 111: 430-443
60. Vass I, Aro EM (2007) Photoinhibition of photosynthetic electron transport. In G Renger, ed, Primary Processes in Photosynthesis, Comprehensive Series in Photochemical and Photobiological Sciences, RSC Publishing, The Royal Society of Chemistry, Cambridge, UK, pp 393-425 part 1
61. Vass I, Kirilovsky D, Etienne A-L (1999) UV-B radiation-induced donorand acceptor-side modifications of photosystem II in the cyanobacterium Synechocystis sp. PCC 6803. Biochemistry 38: 12786-12794
62. Vass I, Styring S, Hundal T, Koivuniemi A, Aro EM, Andersson B (1992) Reversible and irreversible intermediates during photoinhibition of photosystem II: Stable reduced QA species promote chlorophyll triplet formation. Proc Natl Acad Sci USA 89: 1408-1412
63. Vicente JB, Carrondo MA, Teixeira M, Frazão C (2008a) Structural studies on flavodiiron proteins. Methods Enzymol 437: 3-19
64. Vicente JB, Justino MC, Gonçalves VL, Saraiva LM, Teixeira M (2008b) Biochemical, spectroscopic, and thermodynamic properties of flavodiiron proteins. Methods Enzymol 437: 21-45
65. Vicente JB, Testa F, Mastronicola D, Forte E, Sarti P, Teixeira M, Giuffrè A (2009) Redox properties of the oxygen-detoxifying flavodiiron protein from the human parasite Giardia intestinalis. Arch Biochem Biophys 488: 9-13
66. Wasserfallen A, Ragettli S, Jouanneau Y, Leisinger T (1998) A family of flavoproteins in the domains Archaea and Bacteria. Eur J Biochem 254: 325-332
67. Williams JKG (1988) Construction of specific mutations in PSII photosynthetic reaction center by genetic engineering methods in Synechocystis 6803. Methods Enzymol 167: 766-778
68. Wilson A, Ajlani G, Verbavatz JM, Vass I, Kerfeld CA, Kirilovsky D (2006) A soluble carotenoid protein involved in phycobilisome-related energy dissipation in cyanobacteria. Plant Cell 18: 992-1007
69. Winhauer T, Jäger S, Valentin K, Zetsche K (1991) Structural similarities between psbA genes from red and brown algae. Curr Genet 20: 177-180
70. Zhang P, Allahverdiyeva Y, Eisenhut M, Aro EM (2009) Flavodiiron proteins in oxygenic photosynthetic organisms: photoprotection of photosystem II by Flv2 and Flv4 in Synechocystis sp. PCC 6803. PLoS ONE 4: e5331
71. Zhang P, Eisenhut M, Brandt AM, Carmel D, Silén HM, Vass I, Allahverdiyeva Y, Salminen TA, Aro EM (2012) Operon flv4-flv2 provides cyanobacterial photosystem II with flexibility of electron transfer. Plant Cell 24: 1952-1971