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

Photosynthesis Research

Volumn 130, Issue 1-3, 2016, Pages 293-305

  Shimakawa, Ginga ^a   Akimoto, Seiji ^a   Ueno, Yoshifumi ^a   Wada, Ayumi ^a   Shaku, Keiichiro ^a   Takahashi, Yuichiro ^b   Miyake, Chikahiro ^a  

^a KOBE UNIVERSITY   (Japan)

^b OKAYAMA UNIVERSITY   (Japan)

Author keywords

Alternative electron flow; Non photochemical quenching; Photosynthetic electron transport; Species diversity

Indexed keywords

CARBON DIOXIDE; CHLOROPHYLL;

CHLAMYDOMONAS REINHARDTII; ELECTRON TRANSPORT; FLUORESCENCE; METABOLISM; PHOTOSYNTHESIS; PHYSIOLOGY; SYNECHOCOCCUS;

CARBON DIOXIDE; CHLAMYDOMONAS REINHARDTII; CHLOROPHYLL; ELECTRON TRANSPORT; FLUORESCENCE; PHOTOSYNTHESIS; SYNECHOCOCCUS;

EID: 84962301166     PISSN: 01668595     EISSN: 15735079     Source Type: Journal    
DOI: 10.1007/s11120-016-0253-y     Document Type: Article

References (69)

1. 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
2. Appel J, Phunpruch S, Steinmüller K, Schulz R (2000) The bidirectional hydrogenase of Synechocystis sp. PCC 6803 works as an electron valve during photosynthesis. Microbiology 173:333–378
3. Arnon DI, Allen MB, Whatley FR (1954) Photosynthesis by isolated chloroplasts. Nature 1174:394396
4. Asada K (1999) The water-water cycle in chloroplasts: scavenging of active oxygens and dissipation of excess photons. Annu Rev Plant Physiol Plant Mol Biol 50:601–639
5. Beardall J, Quigg A, Raven JA (2003) Oxygen consumption: photorespiration and chlororespiration. In: Larkum WD, Douglas SE, Raven JA (eds) Photosynthesis in algae. Kluwer Academic Publishers, Dordrecht, pp 157–181
6. 6 f complex. In: Peschek G, Obinger C, Renger G (eds) Bioenergetic processes of cyanobacteria. Springer, Dordrecht, pp 573–606
7. Birmingham BC, Coleman JR, Colman B (1982) Measurement of photorespiration in algae. Plant Physiol 69:259–262
8. Campbell D, Hurry V, Clarke AK, Gustafsson P, Öquist G (1998) Chlorophyll fluorescence analysis of cyanobacterial photosynthesis and acclimation. Microbiol Mol Biol Rev 62:667–683
9. Demmig-Adams B, Garab G, Adams III, Govindjee W (eds) (2014) Non-photochemical quenching and energy dissipation in plants, algae and cyanobacteria. Springer, Dordrecht
10. Dvořák P, Casamatta DA, Poulíčková A, Hašler P, Ondřej V, Sanges R (2014) Synechococcus: 3 billion years of global dominance. Mol Ecol 23:5538–5551
11. Eisenhut M, Ruth W, Haimovich M, Bauwe H, Kaplan A, Hagemann M (2008) The photorespiratory glycolate metabolism is essential for cyanobacteria and might have been conveyed endosymbiontically to plants. Proc Natl Acad Sci USA 105:17199–17204
12. Falkowski PG, Fujita Y, Ley A, Mauzerall D (1986) Evidence for cyclic electron flow around photosystem II in Chlorella pyrenoidosa. Plant Physiol 81:310–312
13. Flores E, Frías JE, Rubio LM, Herrero A (2005) Photosynthetic nitrate assimilation in cyanobacteria. Photosynth Res 83:117–133
14. Fujimori T, Hihara Y, Sonoike K (2005) PsaK2 subunit in photosystem I is involved in state transition under high light condition in the cyanobacterium Synechocystis sp. PCC 6803. J Biol Chem 280:22191–22197
15. Fujisawa T, Okamoto S, Katayama T, Nakao M, Yoshimura H, Kajiya-Kanegae H, Yamamoto S, Yano C, Yanaka Y, Maita H, Kaneko T, Tabata S, Nakamura Y (2014) CyanoBase and RhizoBase: databases of manually curated annotations for cyanobacterial and rhizobial genomes. Nucl Acids Res 42:666–670
16. Govindjee Björn LO (2015) Dissecting oxygenic photosynthesis: The evolution of the “Z”-scheme for thylakoid reactions. In: Itoh S, Mohanty P, Guruprasad KN (eds) Photosynthesis: overviews on recent progress and future perspective. Publishers, New Delhi, I.K, pp 1–27
17. Govindjee Amesz J, Fork DC (eds) (1986) Light emission by plants and bacteria. Academic Press, NY
18. 1 obtained from the green alga Chlorella fuska. Biochem Biophys Res Commun 49:1617–1623
19. 2-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
20. 2 in cyanobacteria. Curr Biol 13:230–235
21. Helman Y, Barkan E, Eisenstadt D, Luz B, Kaplan A (2005) Fractionation of the three stable oxygen isotopes by oxygen-producing and oxygen-consuming reactions in photosynthetic organisms. Plant Physiol 138:2292–2298
22. Hihara Y, Kamei A, Kanehisa M, Kaplan A, Ikeuchi M (2001) DNA microarray analysis of cyanobacterial gene expression during acclimation to high light. Plant Cell 13:793–806
23. 2 compensation point and re-supplied with DIC. Photosynth Res 119:257–272
24. 2 environment revealed by fluorescence quenching in photoautotrophically grown Chlamydomonas reinhardtii. Photosynth Res 94:307–314
25. Jordan DB, Ogren WL (1981) Species variation in the specificity of ribulose bisphosphate carboxylase/oxygenase. Nature 291:513–515
26. +-absorbance changes at 830 nm. Planta 192:261–268
27. Klughammer C, Schreiber U (2008) Saturation pulse method for assessment of energy conversion in PSI. PAM Appl Notes 1:11–14
28. Kodru S, Malavath T, Devadasu E, Nellaepalli S, Stirbet A, Subramanyam R, Govindjee (2015) The slow S to M rise of chlorophyll a fluorescence reflects transition from state 2 to state 1 in the green alga Chlamydomonas reinhardtii. Photosynth Res 125:219–231
29. Krieger-Liszkay A (2005) Singlet oxygen production in photosynthesis. J Exp Bot 56:337–346
30. Kusama Y, Inoue S, Jimbo H, Takaichi S, Sonoike K, Hihara Y, Nishiyama Y (2015) Zeaxanthin and echinenone protect the repair of photosystem II from inhibition by singlet oxygen in Synechocystis sp. PCC 6803. Plant Cell Physiol 56:906–916
31. Ley AC, Butler WL (1980) Energy distribution in the photochemical apparatus of Porphyridium cruentum in state I and state II. Biochim Biophys Acta 592:349–363
32. Lichtenthaler HK, Buchanan BB, Douce R, Govindjee (2015) Andrew A. Benson, 1917–2015. Photosynth Res 124:131–135
33. 2 in Chlamydomonas reinhardtii. Plant Physiol 97:420–425
34. McConnell MD, Koop R, Vasil’ev S, Bruce S (2002) Regulation of the distribution of chlorophyll and phycobilin-absorbed excitation energy in cyanobacteria. A structure-based model for the light state transition. Plant Physiol 130:1201–1212
35. Mehler AH (1951) Studies on reactivities of illuminated chloroplasts. I. Mechanism of the reduction of oxygen and other Hill reagents. Arch Biochem Biophys 33:65–77
36. Miller AG, Espie GS, Bruce D (1996) 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
37. Miyake C (2010) 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
38. Miyake C, Asada K (2003) The water-water cycle in algae. In: Larkum WD, Douglas SE, Raven JA (eds) Photosynthesis in algae. Kluwer Academic Publishers, Dordrecht, pp 183–204
39. Miyake C, Yokota A (2001) Cyclic flow of electrons within PSII in thylakoid membranes. Plant Cell Physiol 42:508–515
40. 2 response of cyclic electron flow around PSI (CEF-PSI) in tobacco leaves—relative electron fluxes through PSI and PSII determine the magnitude of non-photochemical quenching (NPQ) of Chl fluorescence. Plant Cell Physiol 46:629–637
41. Moroney JV, Wilson BJ, Tolbert NE (1986) Glycolate metabolism and excretion by Chlamydomonas reinhardtii. Plant Physiol 82:821–826
42. Murata N (1969) Control of excitation transfer in photosynthesis. I. Light-induced change of chlorophyll a fluorescence in Porphyridium cruentum. Biochim Biophys Acta 172:242–251
43. Murchie EH, Lawson T (2013) Chlorophyll fluorescence analysis: a guide to good practice and understanding some new applications. J Exp Bot 64:3983–3998
44. Najafpour M, Moghaddam AN, Shen J-R, Govindjee (2013) Water oxidation and water oxidizing complex in cyanobacteria. In: Srivastava A et al (eds) Stress biology of cyanobacteria. Taylor & Francis, UK, pp 41–60
45. Niyogi KK, Truong TB (2013) Evolution of flexible non-photochemical quenching mechanisms that regulate light harvesting in oxygenic photosynthesis. Curr Opin Plant Biol 16:307–314
46. Papageorgiou GC, Govindjee (eds) (2004) Chlorophyll a fluorescence: a signature of photosynthesis. Advances in Photosynthesis and Respiration, Springer, Dordrecht
47. Papageorgiou GC, Govindjee (2011) Photosystem II fluorescence: slow changes-Scaling from the past. J Photochem Photobiol B 104:258–270
48. Papageorgiou GC, Tsimilli-Michael M, Stamatakis K (2007) The fast and slow kinetics of chlorophyll a fluorescence induction in plants, algae and cyanobacteria: a viewpoint. Photosynth Res 94:275–290
49. 2 availability. Plant J 81:759–766
50. Satoh S, Mimuro M, Tanaka A (2013) Construction of a phylogenetic tree of photosynthetic prokaryotes based on average similarities of whole genome sequences. PLoS One 8:e70290
51. Schreiber U, Schliwa U, Bilger W (1986) Continuous recording of photochemical and non-photochemical chlorophyll fluorescence quenching with a new type of modulation fluorometer. Photosynth Res 10:51–62
52. Schuurmans RM, van Alphen P, Schuurmans JM, Matthijs HCP, Hellingwerf KJ (2015) Comparison of the photosynthetic yield of cyanobacteria and green algae: different methods give different answers. PLoS One 10:e0139061
53. Sejima T, Takagi D, Fukayama H, Makino A, Miyake C (2014) Repetitive short-pulse light mainly inactivates photosystem I in sunflower leaves. Plant Cell Physiol 55:1184–1193
54. 2-uptake is driven by photorespiration in tobacco leaves. Physiol Plant 156:227–238
55. Shaku K, Shimakawa G, Hashiguchi M, Miyake C (2015) Reduction-induced suppression of electron flow (RISE) in the photosynthetic electron transport system of Synechococcus elongatus PCC 7942. Plant Cell Physiol. doi:10.1093/pcp/pcv198
56. Shikanai T (2016) Regulatory network of proton motive force: contribution of cyclic electron transport around photosystem I. Photosynth Res. doi:10.1007/s11120-016-0227-0
57. 2-limited conditions. Plant Physiol 167:472–480
58. Stevens SE, Porter RD (1980) Transformation in Agmenellum quadruplicatum. Proc Natl Acad Sci USA 77:6052–6056
59. Sueoka N (1960) Mitotic replication of deoxyribonucleic acid in Chlamydomonas reinhardtii. Planta 228:1055–1066
60. 2 transport by the green alga Chlamydomonas reinhardtii. Plant Physiol 89:1213–1219
61. Turner S, Pryer KM, Miao VPW, Palmer JD (1999) Investigating deep phylogenetic relationships among cyanobacteria and plastids by small subunit rRNA sequence analysis. J Eukaryot Microbiol 46:327–338
62. van Kooten O, Snel JFH (1990) The use of chlorophyll fluorescence nomenclature in plant stress physiology. Photosynth Res 25:147–150
63. van Thor JJ, Mullineaux CW, Matthijs HCP, Hellingwerf KJ (1998) Light harvesting and state transitions in cyanobacteria. Bot Acta 111:430–443
64. Vicente JB, Gomes CM, Wasserfallen A, Teixeira M (2002) Module fusion in an A-type flavoprotein from the cyanobacterium Synechocystis condenses a multiple-component pathway in a single polypeptide chain. Biochem Biophys Res Commun 294:82–87
65. 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
66. 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
67. Zhou J-J, Fernández E, Galván A, Miller AJ (2000) A high affnity nitrate transport system from Chlamydomonas requires two gene products. FEBS Lett 466:225–227
68. 2 assimilation and photoprotection in wheat leaves. Photosynth Res 126:449–463
69. Zivcak M, Brestic M, Kunderlikova K, Olsovska K, Allakhverdiev SI (2015b) Effect of photosystem I inactivation on chlorophyll a fluorescence induction in wheat leaves: does activity of photosystem I play any role in OJIP rise? J Photochem Photobiol B 152:318–324