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The chlorophyll a fluorescence induction curve in the green microalga Haematococcus pluvialis: further insight into the nature of the P–S–M fluctuation and its relationship with the “low-wave” phenomenon at steady-state

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Abstract

Chlorophyll fluorescence is an information-rich signal which provides an access to the management of light absorbed by PSII. A good example of this is the succession of fast fluorescence fluctuations during light-induced photosynthetic induction after dark-adaptation. During this period, the fluorescence trace exhibits several inflexion points: O–J–I–P–S–M–T. Whereas the OJIP part of this kinetics has been the subject of many studies, the processes that underly the PSMT transient are less understood. Here, we report an analysis of the PSMT phase in the green microalga Haematococcus pluvialis in terms of electron acceptors and light use by photochemistry, fluorescence and non-photochemical quenching (NPQ). We identify additional sub-phases between P and S delimited by an inflexion point, that we name Q, found in the second time scale. The P–Q phase expresses a transient photochemical quenching specifically due to alternative electron transport to oxygen. During the transition from Q to S, the NPQ increases and then relaxes during the S–M phase in about 1 min. It is suggested that this transient NPQ observed during induction is a high energy state quenching (qE) dependent on the alternative electron transport to molecular oxygen. We further show that this NPQ is of the same nature than the NPQ, known as the low-wave phenomenon, which is transiently observed after a saturating light pulse given at steady-state. In both cases, the NPQ is oxygen-dependent. This NPQ is observed at external pH 6.0, but not at pH 7.5, which seems correlated with faster saturation of the PQ pool at pH 6.0.

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References

  • Baker NR (2008) Chlorophyll fluorescence: a probe of photosynthesis in vivo. Annu Rev Plant Biol 59(1):89–113

    Article  CAS  PubMed  Google Scholar 

  • Bannister T, Rice G (1968) Parallel time courses of oxygen evolution and chlorophyll fluorescence. Biochim Biophys Acta (BBA) 162(4):555–580

    Article  CAS  Google Scholar 

  • Bradbury M, Baker NR (1981) Analysis of the slow phases of the in vivo chlorophyll fluorescence induction curve. Changes in the redox state of photosystem II electron acceptors and fluorescence emission from photosystems I and II. Biochim Biophys Acta (BBA) 635(3):542–551

    Article  CAS  Google Scholar 

  • Bulté L, Gans P, Rebéillé F, Wollman FA (1990) ATP control on state transitions in vivo in Chlamydomonas reinhardtii. Biochim Biophys Acta (BBA) 1020(1):72–80

    Article  Google Scholar 

  • Cardol P, Gloire G, Havaux M, Remacle C, Matagne R, Franck F (2003) Photosynthesis and state transitions in mitochondrial mutants of Chlamydomonas reinhardtii affected in respiration. Plant Physiol 133(4):2010–2020

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cardol P, De Paepe R, Franck F, Forti G, Finazzi G (2010) The onset of NPQ and Δμ H + upon illumination of tobacco plants studied through the influence of mitochondrial electron transport. Biochim Biophys Acta (BBA) 1797(2):177–188

    Article  CAS  Google Scholar 

  • de Marchin T (2015) From photons to biomass in green microalgae: fluorimetric and oximetric studies on the regulation of photosynthetic electron transport. Ph.D. thesis

  • Delosme R, Olive J, Wollman FA (1996) Changes in light energy distribution upon state transitions: an in vivo photoacoustic study of the wild type and photosynthesis mutants from Chlamydomonas reinhardtii. Biochim Biophys Acta 1273(2):150–158

    Article  Google Scholar 

  • Development Core Team R (2008) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  • Finazzi G, Minagawa J (2014) High light acclimation in green microalgae in non-photochemical quenching and thermal energy dissipation in plants, algae and cyanobacteria. Adv Photosynth Respir Incl Bioenergy Relat Process 40:24

    Google Scholar 

  • Finazzi G, Johnson GN, Dallosto L, Joliot P, Wollman FA, Bassi R (2004) A zeaxanthin-independent non-photochemical quenching mechanism localized in the photosystem II core complex. Proc Natl Acad Sci USA 101(33):12375–12380

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Franck F, Houyoux PA (2008) The mehler reaction in Chlamydomonas during photosynthetic induction and steady-state photosynthesis in wild-type and in a mitochondrial mutant. In: Photosynthesis. Energy from the Sun. Springer, The Netherlands, pp 581–584

  • Genty B, Briantais JM, Baker NR (1989) The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochim Biophys Acta (BBA) 990(1):87–92

    Article  CAS  Google Scholar 

  • Hendrickson L, Furbank RT, Chow WS (2004) A simple alternative approach to assessing the fate of absorbed light energy using chlorophyll fluorescence. Photosynth Res 82(1):73–81

    Article  CAS  PubMed  Google Scholar 

  • Houille-Vernes L, Rappaport F, Wollman FA, Alric J, Johnson X (2011) Plastid Terminal Oxidase 2 (PTOX2) is the major oxidase involved in chlororespiration in Chlamydomonas. Proc Natl Acad Sci 108(51):20820–20825

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jans F, Mignolet E, Houyoux PA, Cardol P, Ghysels B, Cuiné S, Cournac L, Peltier G, Remacle C, Franck F (2008) A type II NAD(P)H dehydrogenase mediates light-independent plastoquinone reduction in the chloroplast of Chlamydomonas. Proc Natl Acad Sci 105(51):20546–20551

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jassby AD (1976) Mathematical formulation of the relationship between photosynthesis and light for phytoplankton. Limnol Oceanogr 21:540–547

    Article  CAS  Google Scholar 

  • Johnson X, Alric J (2012) Interaction between starch breakdown, acetate assimilation, and photosynthetic cyclic electron flow in Chlamydomonas Reinhardtii. J Biol Chem 287(31):26445–26452

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Joliot P, Lavorel J (1964) Les réactions primaires de la photosynthèse. Bulletin de La Société de Chimie Biologique 46(12):1607

    CAS  PubMed  Google Scholar 

  • Kalituho L, Beran KC, Jahns P (2007) The transiently generated non-photochemical quenching of excitation energy in Arabidopsis leaves is modulated by zeaxanthin. Plant Physiol 143(4):1861–1870

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kautsky H, Hirsch A (1931) Neue versuche zur kohlensäureassimilation. Naturwissenschaften 19(48):964–964

    Article  CAS  Google Scholar 

  • 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, 1–13

  • Larcher W, Neuner G (1989) Cold-induced sudden reversible lowering of in vivo chlorophyll fluorescence after saturating light pulses a sensitive marker for chilling susceptibility. Plant Physiol 89(3):740–742

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lichtenthaler HK (1987) Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. Methods Enzymol 148:350–382

    Article  CAS  Google Scholar 

  • Makino A, Miyake C, Yokota A (2002) Physiological functions of the water–water cycle (Mehler reaction) and the cyclic electron flow around PSI in rice Leaves. Plant Cell Physiol 43(9):1017–1026

    Article  CAS  PubMed  Google Scholar 

  • Maxwell K, Johnson GN (2000) Chlorophyll fluorescence—a practical guide. J Exp Bot 51(345):659–668

    Article  CAS  PubMed  Google Scholar 

  • McConnell IL, Eaton-Rye JJ, Rensen JJ (2012) Regulation of photosystem II electron transport by bicarbonate. In: Photosynthesis. Springer, The Netherlands, pp 475–500

  • Miller AG, Canvin DT (1989) Glycolaldehyde inhibits CO2 fixation in the cyanobacterium Synechococcus UTEX 625 without inhibiting the accumulation of inorganic carbon or the associated quenching of chlorophyll a fluorescence. Plant Physiol 91(3):1044–1049

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Miyake C, Asada K (2003) The water-water cycle in algae. In: Larkum AWD, Douglas SE, Raven JA (eds) Photosynthesis in Algae. Springer, The Netherlands, pp 183–204

  • Neubauer C, Schreiber U (1987) The polyphasic rise of chlorophyll fluorescence upon onset of strong continuous illumination: I. Saturation characteristics and partial control by the photosystem II acceptor side. Zeitschrift Fuer Naturforschung C 42c:1246–1254

    Google Scholar 

  • Nichols HW, Bold HC (1965) Trichsarcina Polyinorpha Gen. et Sp. Nov. J Phycol 34–38

  • Papageorgiou G, Govindjee (1971) pH control of the chlorophyll a fluorescence in algae. Biochim Biophys Acta (BBA) 234(3):428–432

    Article  CAS  Google Scholar 

  • 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(2–3):275–290

    Article  CAS  PubMed  Google Scholar 

  • Radmer RJ, Kok B (1976) Photoreduction of O2 primes and replaces CO2 Assimilation. Plant Physiol 58(3):336–340

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Roberty S, Bailleul B, Berne N, Franck F, Cardol P (2014) PSI Mehler reaction is the main alternative photosynthetic electron pathway in Symbiodinium sp. symbiotic dinoflagellates of cnidarians. New Phytol 204(1):81–91

    Article  CAS  PubMed  Google Scholar 

  • Rochaix JD (2014) Regulation and dynamics of the light-harvesting system. Annu Rev Plant Biol 65(1):287–309

    Article  CAS  PubMed  Google Scholar 

  • 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(1–2):51–62

    Article  CAS  PubMed  Google Scholar 

  • 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(5):873–882

    CAS  Google Scholar 

  • Stirbet A, Riznichenko GY, Rubin AB, Govindjee (2014) Modeling chlorophyll a fluorescence transient: relation to photosynthesis. Biochemistry (Moscow) 79(4):291–323

    Article  CAS  Google Scholar 

  • Strasser RJ, Srivastava A (1995) Polyphasic chlorophyll a fluorescence transient in plants and cyanobacteria. Photochem Photobiol 61(1):32–42

    Article  CAS  Google Scholar 

  • Tsuyama M, Shibata M, Kawazu T, Kobayashi Y (2004) An analysis of the mechanism of the low-wave phenomenon of chlorophyll fluorescence. Photosynth Res 81(1):67–76

    Article  CAS  PubMed  Google Scholar 

  • Wydrzynski T, Govindjee (1975) A new site of bicarbonate effect in photosystem II of photosynthesis: evidence from chlorophyll fluorescence transients in spinach chloroplasts. Biochim Biophys Acta (BBA) 387(2):403–408

    Article  CAS  Google Scholar 

  • Xyländer M, Hagen C (2002) Low-waves in chlorophyll fluorescence kinetics indicate deprivation of bicarbonate. Photosynth Res 72(3):255–262

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

AF was the recipient of a fellowship of FRIA, who is acknowledged for its support. This work was financed in part by grant FRFC No. 2.4.631.09. The authors warmly thank Dr Pierre Cardol for helpful advices and discussions. FF is research director of the F.R.S.-FNRS.

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  1. Anthony Fratamico

    Present address: InBioS - Laboratory of Plant Physiology, University of Liège, Quartier Vallée 1, Sart-Tilman Campus, 4 Chemin de la Vallée, Liège, Belgium

Authors and Affiliations

  1. InBioS - Laboratory of Bioenergetics, University of Liège, Quartier Vallée 1, Sart-Tilman Campus, 4 Chemin de la Vallée, Liège, Belgium

    Anthony Fratamico & Fabrice Franck

  2. InBioS - Laboratory of Plant Physiology, University of Liège, Quartier Vallée 1, Sart-Tilman Campus, 4 Chemin de la Vallée, Liège, Belgium

    Pierre Tocquin

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Correspondence to Fabrice Franck.

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11120_2016_241_MOESM1_ESM.png

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Fig. S1 Light-saturation curves of gross steady-state photosynthetic evolution in phototrophically-grown H. pluvialis. Measurements were performed either at pH 6.0 (closed circles, solid line) or at pH 7.5 (open circles, dashed line). Fits were performed using the hyperbolic tangent equation of (Jassby 1976). Error bars indicate standard deviation of three independent experiments

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Fratamico, A., Tocquin, P. & Franck, F. The chlorophyll a fluorescence induction curve in the green microalga Haematococcus pluvialis: further insight into the nature of the P–S–M fluctuation and its relationship with the “low-wave” phenomenon at steady-state. Photosynth Res 128, 271–285 (2016). https://doi.org/10.1007/s11120-016-0241-2

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