Diverse strategies of O2 usage for preventing photo-oxidative damage under CO2 limitation during algal photosynthesis

Scientific Reports

Volumn 7, Issue , 2017, Pages

  Shimakawa, Ginga ^a   Matsuda, Yusuke ^b   Nakajima, Kensuke ^b   Tamoi, Masahiro ^c   Shigeoka, Shigeru ^c   Miyake, Chikahiro ^a  

^a KOBE UNIVERSITY   (Japan)

^b KWANSEI GAKUIN UNIVERSITY   (Japan)

^c KINKI UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CARBON DIOXIDE; OXYGEN;

DIATOM; ELECTRON TRANSPORT; ENERGY METABOLISM; EUGLENA GRACILIS; METABOLISM; OXIDATIVE STRESS; PHOTOSYNTHESIS;

CARBON DIOXIDE; DIATOMS; ELECTRON TRANSPORT; ENERGY METABOLISM; EUGLENA GRACILIS; OXIDATIVE STRESS; OXYGEN; PHOTOSYNTHESIS;

EID: 85010390751     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep41022     Document Type: Article

References (57)

1. Kasting, J. F. Theoretical constraints on oxygen and carbon dioxide concentrations in the Precambrian atmosphere. Precambrian Res. 34, 205-229 (1987).
2. Mitchell, P. Chemiosmotic coupling in oxidative and photosynthetic phosphorylation. Biol. Rev. 41, 445-501 (1966).
3. Trebst, A. Energy conservation in photosynthetic electron transport of chloroplasts. Annu. Rev. Plant Physiol. 25, 423-458 (1974).
4. Murata, N., Takahashi, S., Nishiyama, Y. & Allakhverdiyev, S. I. Photoinhibition of photosystem II under environmental stress. Biophys. Biochim. Acta Bioenerg. 1767, 414-421 (2007).
5. Roach, T., Na, C. S. & Krieger-Liszkay, A. High light-induced hydrogen peroxide production in Chlamydomonas reinhardtii is increased by high CO2 availability. Plant J. 81, 759-766 (2015).
6. Sonoike, K. Photoinhibition of photosystem I. Physiol. Plant. 142, 56-64 (2011).
7. Sejima, T., Takagi, D., Fukayama, H., Makino, A. & Miyake, C. Repetitive short-pulse light mainly inactivates photosystem I in sunflower leaves. Plant Cell Physiol. 55, 1184-1193 (2014).
8. Miyake, C. Alternative electron flows (water-water cycle and cyclic electron flow around PSI) in photosynthesis: molecular mechanisms and physiological functions. Plant Cell Physiol. 51, 1951-1963 (2010).
9. Mehler, A. H. Studies on reactivities of illuminated chloroplasts. I. Mechanism of the reduction of oxygen and other Hill reagents. Arch. Biochem. Biophys. 33, 65-77 (1951).
10. Miyake, C., Schreiber, U., Hormann, H., Sano, S. & Asada, K. The FAD-enzyme monodehydroascorbate radical reductase mediates photoproduction of superoxide radicals in spinach thylakoid membranes. Plant Cell Physiol. 39, 821-829 (1998).
11. Helman, Y. et al. Genes encoding A-Type flavoproteins are essential for photoreduction of O2 in cyanobacteria. Curr. Biol. 13, 230-235 (2003).
12. Hayashi, R. et al. O2-dependent large electron flow functioned as an electron sink, replacing the steady-state electron flux in photosynthesis in the cyanobacterium Synechocystis sp. PCC 6803, but not in the cyanobacterium Synechococcus sp. PCC 7942. Biosci. Biotechnol. Biochem. 78, 384-393 (2014).
13. Shimakawa, G. et al. FLAVODIIRON2 and FLAVODIIRON4 proteins mediate and oxygen-dependent alternative electron flow in Synechocystis sp. PCC 6803 under CO2-limited conditions. Plant Physiol. 167, 472-480 (2015).
14. Noguchi, K. & Yoshida, K. Interaction between photosynthesis and respiration in illuminated leaves. Mitochondrion 8, 87-99 (2008).
15. Joët, T. et al. Involvement of a plastid terminal oxidase in plastoquinone oxidation as evidenced by expression of the Arabidopsis thaliana enzyme in tobacco. J. Biol. Chem. 277, 31623-31630 (2002).
16. Lea-Smith, D. J. et al. Thylakoid terminal oxidases are essential for the cyanobacterium Synechocystis sp. PCC 6803 to survive rapidly changing light intensities. Plant Physiol. 162, 484-495 (2013).
17. Kozaki, A. & Takeba, G. Photorespiration protects C3 plants from photooxidation. Nature 384, 557-560 (1996).
18. Sejima, T. et al. Post-illumination transient O2-uptake is driven by photorespiration in tobacco leaves. Physiol. Plant. 156, 227-238 (2016).
19. Takagi, D., Hashiguchi, M., Sejima, T., Makino, A. & Miyake, C. Photorespiration provides the chance of cyclic electron flow to operate for the redox-regulation of P700 in photosynthetic electron transport system of sunflower leaves. Photosynth. Res. doi: 10.1007/s11120-016-0267-5 (2016).
20. Zhang, P., Allahverdiyeva, Y., Eisenhut, M. & Aro, E. M. Flavodiiron proteins in oxygenic photosynthetic organisms: photoprotection of photosystem II by Flv2 and Flv4 in Synechocystis sp. PCC 6803. PLoS One 4, e5331 (2009).
21. Allahverdiyeva, Y. et al. Flavodiiron proteins Flv1 and Flv3 enable cyanobacterial growth and photosynthesis under fluctuating light. Proc. Natl. Acad. Sci. USA 110, 4111-4116 (2013).
22. Shimakawa, G., Shaku, K. & Miyake, C. Oxidation of P700 in photosystem I is essential for the growth of cyanobacteria. Plant Physiol. doi: http://dx.doi.org/10.1104/pp.16.382 012277 (2016).
23. Shimakawa, G. et al. Diversity in photosynthetic electron transport under [CO2]-limitation: The cyanobacterium Synechococcus sp. PCC 7002 and green alga Chlamydomonas reinhardtii drive an O2-dependent alternative electron flow and non-photochemical quenching of chlorophyll fluorescence during CO2-limited photosynthesis. Photosynth. Res. 130, 293-305 (2016).
24. Goss, R. & Lepetit, B. Biodiversity of NPQ. J. Plant Physiol. 172, 13-32 (2015).
25. Derks, A., Schaven, K. & Bruce, D. Diverse mechanisms for photoprotection in photosynthesis. Dynamic regulation of photosystem II excitation in response to rapid environmental change. Biochim. Biophys. Acta Bioenerg. 1847, 468-485 (2015).
26. Hope, A. B., Valente, P. & Matthews, D. B. Effects of pH on the kinetics of redox reactions in and around the cytochrome bf complex in an isolated system. Photosynth. Res. 42, 111-120 (1994).
27. Shaku, K., Shimakawa, G., Hashiguchi, M. & Miyake, C. Reduction-induced suppression of electron flow (RISE) in the photosynthetic electron transport system of Synechococcus elongatus PCC 7942. Plant Cell Physiol. 57, 1443-1453 (2016).
28. Allen, J. F. Cyclic, pseudocyclic and noncyclic photophosphorylation: new links in the chain. Trends Plant Sci. 8, 15-19 (2003).
29. Peltier, G., Tolleter, D., Billon, E. & Cournac, L. Auxiliary electron transport pathways in chloroplasts of microalgae. Photosynth. Res. 106, 19-31 (2010).
30. Falkowski, P. G., Fujita, Y., Ley, A. & Mauzerall, D. Evidence for cyclic electron flow around photosystem II in Chlorella pyrenoidosa. Plant Physiol. 81, 310-312 (1986).
31. Miyake, C. & Yokota, A. Cyclic flow of electrons within PSII in thylakoid membranes. Plant Cell Physiol 42, 508-515 (2001).
32. Falkowski, P. G. et al. The evolution of modern eukaryotic phytoplankton. Science 305, 354-360 (2004).
33. Cunningham, F. X. Jr. & Schiff, J. A. Chlorophyll-protein complexes from Euglena gracilis and mutants deficient in chlorophyll b. Plant Physiol. 80, 231-238 (1986).
34. Casper-Lindley, C. & Björkman, O. Fluorescence quenching in four unicellular algae with different light-harvesting and xanthophyll-cycle pigments. Photosynth. Res. 56, 277-289 (1998).
35. Campbell, D., Hurry, V., Clarke, A. K., Gustafsson, P. & Öquist, G. Chlorophyll fluorescence analysis of cyanobacterial photosynthesis and acclimation. Microbiol. Mol. Biol. Rev. 62, 667-683 (1998).
36. Miller, A. G., Espie, G. S. & Bruce, D. Characterization of the non-photochemical quenching of chlorophyll fluorescence that occurs during the active accumulation of inorganic carbon in the cyanobacterium Synechococcus PCC 7942. Photosynth. Res. 49, 251-262 (1996).
37. Jordan, D. B. & Ogren, W. L. Species variation in the specificity of ribulose bisphosphate carboxylase/oxygenase. Nature 291, 513-515 (1981).
38. Yokota, A. & Kitaoka, S. Rates of glycolate synthesis and metabolism during photosynthesis of Euglena and microalgae grown on low CO2. Planta 170, 181-189 (1987).
39. Trimborn, S., Thoms, S., Petrou, K., Kranz, S. A. & Rost, B. Photophysiological responses of Southern Ocean phytoplankton to changes in CO2 concentrations: Short-Term versus acclimation effects. J. Exp. Mar. Biol. Ecol. 451, 44-54 (2014).
40. Bailleul, B. et al. Energetic coupling between plastids and mitochondria drives CO2 assimilation in diatoms. Nature 524, 366-369 (2015).
41. Driever, S. M. & Baker, N. R. The water-water cycle in leaves is not a major alternative electron sink for dissipation of excess excitation energy when CO2 assimilation is restricted. Plant Cell Environ. 34, 837-846 (2011).
42. Waring, J., Klenell, M., Bechtold, U., Underwood, G. J. C. & Baker, N. R. Light-induced responses of oxygen photoreduction, reactive oxygen species production and scavenging in two diatom species. J. Phycol. 46, 1206-1217 (2010).
43. Miyake, C., Michihata, F. & Asada, K. Scavenging of hydrogen peroxide in prokaryotic and eukaryotic algae: Acquisition of ascorbate peroxidase during the evolution of cyanobacteria. Plant Cell Physiol. 32, 33-43 (1991).
44. Wilson, A. et al. A soluble carotenoid protein involved in phycobilisome-related energy dissipation in cyanobacteria. Plant Cell 18, 992-1007 (2006).
45. Bailleul, B. et al. An atypical member of the light-harvesting complex stress-related protein family modulates diatom responses to light. Proc. Natl. Acad. Sci. USA 107, 18214-18219 (2010).
46. Richter, P. R. et al. High light exposure leads to a sign change of gravitaxis in the flagellate Euglena gracilis. Acta Protozool. 41, 343-351 (2002).
47. Allen, M. M. Simple conditions for growth of unicellular blue-green algae on plates. J. Phycol. 4, 1-4 (1968).
48. Grimme, L. H. & Boardman, N. K. Photochemical activities of a particle fraction P1 obtained from the green alga Chlorella fuska. Biochem. Biophys. Res. Commun. 49, 1617-1623 (1972).
49. Cramer, M. & Myers, J. Growth and photosynthetic characteristics of Euglena gracilis. Arch. Mikrobiol. 17, 384-402 (1952).
50. Guillard, R. R. L. & Ryther, J. H. Studies of marine planktonic diatoms. I. Cyclotella nana Hustedt and Detonula confervacea (Cleve) Gran. Can. J. Microbiol. 8, 229-239 (1962).
51. Guillard, R. R. L. Culture of phytoplankton for feeding marine invertebrates. In: Smith, W. L. & Chanley, M. H. (eds) Culture of Marine Invertebrate Animals, Plenum Press, New York, pp 29-60 (1975).
52. Jeffrey, S. W. & Humphrey, G. F. New spectrophotometric equations for determining chlorophylls a, b, c1 and c2 in higher plants, algae and natural phytoplankton. Biochem. Physiol. Pflanz. 167, 191-194 (1975).
53. Schreiber, U., Schliwa, U. & Bilger, W. Continuous recording of photochemical and non-photochemical chlorophyll fluorescence quenching with a new type of modulation fluorometer. Photosynth. Res. 10, 51-62 (1986).
54. Genty, B., Briantais, J. M. & Baker, N. R. The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochim. Biophys. Acta Gen. Subj. 990, 87-92 (1989).
55. van Kooten, O. & Snel, J. F. H. The use of chlorophyll fluorescence nomenclature in plant stress physiology. Photosynth. Res. 25, 147-150 (1990).
56. Baker, N. R. Chlorophyll fluorescence: A probe of photosynthesis in vivo. Annu. Rev. Plant Biol. 59, 89-113 (2008).
57. Shimakawa, G. et al. Respiration accumulates Calvin cycle intermediates for the rapid start of photosynthesis in Synechocystis sp. PCC 6803. Biosci. Biotechnol. Biochem. 78, 1997-2007 (2014).