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Application of spectrally resolved fluorescence induction to study light-induced nonphotochemical quenching in algae

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  • Published:
Photosynthetica

Abstract

The light-induced nonphotochemical quenching (NPQ) can safely dissipate excess of absorbed light to heat. Here we describe an application of spectrally resolved fluorescence induction (SRFI) method for studying spectral variability of NPQ. The approach allows detection of spectrally-resolved nonphotochemical quenching (NPQλ) representing NPQ dependency on fluorescence emission wavelength in the whole spectral range of fluorescence emission. The experimental approach is briefly described and NPQλ is studied for the cryptophyte alga Rhodomonas salina and for green alga Chlorella sp. We confirm presence of NPQλ only in membrane-bound antennae (chlorophyll a/c antennae) and not in phycobiliproteins in lumen in cryptophyte and show that NPQλ is inhibited in the whole spectral range by NPQ inhibitors in Chlorella sp. We discuss variability in the quenching in the particular spectral ranges and applicability of the NPQλ parameter to study quenching locus in vivo.

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Abbreviations

CAC:

chlorophyll a/c antennae complexes of cryptophyte

Chl:

chlorophyll

DCMU:

3-(3,4-dichlorophenyl)-1,1-dimethylurea

Ft :

fluorescence intensity at particular irradiance/time of measuring protocol

F0 :

minimal fluorescence intensity for open reaction center

FM :

maximal fluorescence intensity for closed reaction center measured with dark-adapted sample

FM‘ :

maximal fluorescence intensity for closed reaction center measured with light-adapted sample

NPQ:

nonphotochemical quenching of chlorophyll a fluorescence

NPQλ :

spectrally resolved nonphotochemical quenching of fluorescence

RC:

reaction center

Rfd:

fluorescence decrease ratio

References

  • Acuña A.M., Kaňa R., Gwizdala M. et al: Synechocystis PCC 6803 during lightinduced state transitions.–Photosynth. Res. 130: 237–249, 2016.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Belgio E., Duffy C.D.P., Ruban A.V.: Switching light harvesting complex II into photoprotective state involves the lumen-facing apoprotein loop.–Phys. Chem. Chem. Phys. 15: 12253–12261, 2013.

    Article  PubMed  CAS  Google Scholar 

  • Belgio E., Kapitonova E., Chmeliov J. et al.: Economic photoprotection in photosystem II that retains a complete lightharvesting system with slow energy traps.–Nat. Commun. 5: 4433, 2014.

    Article  PubMed  CAS  Google Scholar 

  • Bernat G., Steinbach G., Kaňa R. et al.: On the origin of the slow M to T chlorophyll a fluorescence decline in cyanobacteria: interplay of short-term light-responses.–Photosynth. Res. DOI: 10.1007/s11120-017-0458-8, in press, 2018.

    Google Scholar 

  • Bilger W., Björkman O.: Role of the xanthophyll cycle in photoprotection elucidated by measurements of light-induced absorbancy changes, fluorescence and photosynthesis in leaves of Hedera canariensis.–Photosynth. Res. 25: 173–185, 19

    Article  PubMed  CAS  Google Scholar 

  • Briantais J.M., Vernotte C., Picaud M. et al.: Quantitative study of the slow decline of chlorophyll alpha-fluorescence in isolated-chloroplasts.–Biochim. Biophys. Acta 548: 128–138, 1979.

    Article  PubMed  CAS  Google Scholar 

  • Bruce D., Samson G., Carpenter C.: The origins of nonphotochemical quenching of chlorophyll fluorescence in photosynthesis. Direct quenching by P680+ in photosystem II enriched membranes at low pH.–Biochemistry 36: 749–755, 1997.

    Article  PubMed  CAS  Google Scholar 

  • Büchel C.: Evolution and function of light harvesting proteins.–J. Plant Physiol. 172: 62–75, 2015.

    Article  PubMed  CAS  Google Scholar 

  • Cheregi O., Kotabová E., Prášil O. et al.: Presence of state transitions in the cryptophyte alga Guillardia theta.–J. Exp. Bot. 66: 6461–6470, 2015.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Cser K., Vass I.: Radiative and non-radiative charge recombination pathways in Photosystem II studied by thermoluminescence and chlorophyll fluorescence in the cyanobacterium Synechocystis 6803.–BBA-Bioenergetics 1767: 233–243, 2007.

    Article  PubMed  CAS  Google Scholar 

  • Delphin E., Duval J.C., Etienne A.L. et al.: Delta pH-dependent photosystem II fluorescence quenching induced by saturating, multiturnover pulses in red algae.–Plant Physiol. 118: 103–113, 1998.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Demmig-Adams B., Garab G., Adams III W. et al.: Non-Photochemical Quenching and Energy Dissipation in Plants, Algae and Cyanobacteria. Springer, Dordrecht 2014.

    Google Scholar 

  • Derks A., Schaven K., Bruce D.: Diverse mechanisms for photoprotection in photosynthesis. Dynamic regulation of photosystem II excitation in response to rapid environmental change.–BBA-Bioenergetics 1847: 468–485, 2015.

    Article  PubMed  CAS  Google Scholar 

  • Franck F., Dewez D., Popovic R.: Changes in the roomtemperature emission spectrum of chlorophyll during fast and slow phases of the Kautsky effect in intact leaves.–Photoch. Photobio. 81: 431–436, 2005.

    Article  CAS  Google Scholar 

  • Franck F., Juneau P., Popovic R.: Resolution of the Photosystem I and Photosystem II contributions to chlorophyll fluorescence of intact leaves at room temperature.–BBA-Bioenergetics 1556: 239–246, 2002.

    Article  PubMed  CAS  Google Scholar 

  • Funk C., Alami M., Tibiletti T. et al.: High light stress and the one-helix LHC-like proteins of the cryptophyte Guillardia theta.–BBA-Bioenergetics 1807: 841–846, 20

    Article  PubMed  CAS  Google Scholar 

  • Gilmore A.M., Yamamoto H.Y.: Dark induction of zeaxanthindependent nonphotochemical fluorescence quenching mediated by ATP.–P. Natl. Acad. Sci. USA 89: 1899–1903, 1992.

    Article  CAS  Google Scholar 

  • Giovagnetti V., Ware M.A., Ruban A.V.: Assessment of the impact of photosystem I chlorophyll fluorescence on the pulseamplitude modulated quenching analysis in leaves of Arabidopsis thaliana.–Photosynth. Res. 125: 179–189, 20

    Article  PubMed  CAS  Google Scholar 

  • Holzwarth A.R., Lenk D., Jahns P.: On the analysis of nonphotochemical chlorophyll fluorescence quenching curves: I. Theoretical considerations.–BBA-Bioenergetics 1827: 786–792, 2013.

    Article  PubMed  CAS  Google Scholar 

  • Holzwarth A.R., Miloslavina Y., Nilkens M. et al.: Identification of two quenching sites active in the regulation of photosynthetic light-harvesting studied by time-resolved fluorescence.–Chem. Phys. Lett. 483: 262–267, 2009.

    Article  CAS  Google Scholar 

  • Johnson M.P., Ruban A.V.: Photoprotective Energy dissipation in higher plants involves alteration of the excited state energy of the emitting chlorophyll(s) in the light harvesting antenna II (LHCII).–J. Biol. Chem. 284: 23592–23601, 2009.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kaftan D., Trtilek M., Kroon B. et al.: Fast-response doublemodulation fluorometer.–In: Garab G. (ed.): International Congress on Photosynthesis, Vol. 5. Pp. 4297–4300. Kluwer Academic Publishers, Budapest 1997.

    Google Scholar 

  • Kaňa R., Govindjee: Role of ions in the regulation of lightharvesting.–Front. Plant Sci. 7: 1849, 2016.

    Article  PubMed  PubMed Central  Google Scholar 

  • Kaňa R., Kotabová E., Komárek O. et al.: The slow S to M fluorescence rise in cyanobacteria is due to a state 2 to state 1 transition.–BBA-Bioenergetics 1817: 1237–1247, 2012a.

    Article  PubMed  CAS  Google Scholar 

  • Kaňa R., Kotabová E., Kopečná J. et al.: Violaxanthin inhibits nonphotochemical quenching in light-harvesting antenna of Chromera velia.–FEBS Lett. 590: 1076–1085, 2016.

    Article  PubMed  CAS  Google Scholar 

  • Kaňa R., Kotabová E., Sobotka R. et al.: Non-photochemical quenching in cryptophyte alga Rhodomonas salina is located in chlorophyll a/c antennae.–PLoS ONE 7: e29700, 2012b.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kaňa R., Prášil O., Komárek O. et al.: Spectral characteristic of fluorescence induction in a model cyanobacterium, Synechococcus sp (PCC 7942).–Biochim. Biophys. Acta 1787: 1170–1178, 2009a.

    Article  PubMed  CAS  Google Scholar 

  • Kaňa R., Prášil O., Mullineaux C.W.: Immobility of phycobilins in the thylakoid lumen of a cryptophyte suggests that protein diffusion in the lumen is very restricted.–FEBS Lett. 583: 670–674, 2009b.

    Article  PubMed  CAS  Google Scholar 

  • Kaňa R., Vass I.: Thermoimaging as a tool for studying lightinduced heating of leaves: Correlation of heat dissipation with the efficiency of photosystem II photochemistry and nonphotochemical quenching.–Environ. Exp. Bot. 64: 90–96, 2008.

    Article  Google Scholar 

  • Komura M., Yamagishi A., Shibata Y. et al.: Mechanism of strong quenching of photosystem II chlorophyll fluorescence under drought stress in a lichen, Physciella melanchla, studied by subpicosecond fluorescence spectroscopy.–BBABioenergetics 1797: 331–338, 2010.

    Article  CAS  Google Scholar 

  • Kotabová E., Jarešova J., Kaňa R. et al.: Novel type of red-shifted chlorophyll a antenna complex from Chromera velia. I. Physiological relevance and functional connection to photosystems.–Biochim. Biophys. Acta 1837: 734–743, 2014.

    Article  PubMed  CAS  Google Scholar 

  • Kotabová E., Kaňa R., Jarešova J. et al.: Non-photochemical fluorescence quenching in Chromera velia is enabled by fast violaxanthin de-epoxidation.–FEBS Lett. 585: 1941–1945, 2011.

    Article  PubMed  CAS  Google Scholar 

  • Kramer D.M., Johnson G., Kiirats O. et al.: New fluorescence parameters for the determination of QA redox state and excitation energy fluxes.–Photosynth. Res. 79: 209–218, 2004.

    Article  PubMed  CAS  Google Scholar 

  • Krüger T.P.J., Ilioaia C., Johnson M.P. et al.: The specificity of controlled protein disorder in the photoprotection of plants.–Biophys. J. 105: 1018–1026, 2013.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Krüger T.P.J., Wientjes E., Croce R. et al.: Conformational switching explains the intrinsic multifunctionality of plant light-harvesting complexes.–P. Natl. Acad. Sci. USA 108: 13516–13521, 2011.

    Article  Google Scholar 

  • Krupnik T., Kotabová E., van Bezouwen L.S. et al.: A reaction centre-dependent photoprotection mechanism in a highly robust photosystem II from an extremophilic red alga Cyanidioschyzon merolae.–J. Biol. Chem. 288: 23529–23542., 2013.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kulasek M., Bernacki M.J., Ciszak K. et al.: Contribution of PsbS Function and stomatal conductance to foliar temperature in higher plants.–Plant Cell Physiol. 57: 1495–1509, 2016.

    PubMed  PubMed Central  CAS  Google Scholar 

  • Lakowicz J.R.: Principles of Fluorescence Spectroscopy. Springer, New York 2006.

    Book  Google Scholar 

  • Lambrev P.H., Nilkens M., Miloslavina Y. et al.: Kinetic and spectral resolution of multiple nonphotochemical quenching components in Arabidopsis leaves.–Plant Physiol. 152: 1611–1624, 2010.

    Article  PubMed  CAS  Google Scholar 

  • Lazár D.: Simulations show that a small part of variable chlorophyll a fluorescence originates in photosystem I and contributes to overall fluorescence rise.–J. Theor. Biol. 335: 249–264, 2013.

    Article  PubMed  CAS  Google Scholar 

  • Lazár D.: Parameters of photosynthetic energy partitioning.–J. Plant Physiol. 175: 131–147, 2015.

    Article  PubMed  CAS  Google Scholar 

  • Li X.P., Björkman O., Shih C. et al: A pigment-binding protein essential for regulation of photosynthetic light harvesting.–Nature 403: 391–395, 2000.

    Article  PubMed  CAS  Google Scholar 

  • MacPherson A.N., Hiller R.G.: Algae with chlorophyll c in lightharvesting antennae in photosynthesis.–In: Green B.R. and Parson W.W. (ed.): Light-Harvesting Antennas in Photosynthesis. Pp. 323–352. Kluwer Acad. Publ., Dordrecht 2003.

    Chapter  Google Scholar 

  • Miloslavina Y., Wehner A., Lambrev P.H. et al.: Far-red fluorescence: A direct spectroscopic marker for LHCII oligomer formation in non-photochemical quenching.–FEBS Lett. 582: 3625–3631, 2008.

    Article  PubMed  CAS  Google Scholar 

  • Miyake H., Komura M., Itoh S. et al.: Multiple dissipation components of excess light energy in dry lichen revealed by ultrafast fluorescence study at 5 K.–Photosynth. Res. 110: 39–48, 2011.

    Article  PubMed  CAS  Google Scholar 

  • Niyogi K.K., Björkman O., Grossman A.R.: The roles of specific xanthophylls in photoprotection.–P. Natl. Acad. Sci. USA 94: 14162–14167, 1997.

    Article  CAS  Google Scholar 

  • Novotný J.P., Chugtai A.A., Kostrouchová M. et al.: Trichoplax adhaerens reveals a network sensitive to 9-cis-retinoic acid at the base of metazoan evolution.–Peer J. 5: e3789, 2017.

    Article  PubMed  Google Scholar 

  • Ohad I., Raanan H., Keren N. et al.: Light-Induced changes within photosystem ii protects microcoleus sp in biological desert sand crusts against excess light.–PLoS ONE 5: e11000, 2010.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Papageorgiou G.C., Govindjee: Chlorophyll a Fluorescence. A Signature of Photosynthesis. Springer, Dordrecht 2004.

    Book  Google Scholar 

  • Passarini F., Wientjes E., van Amerongen H. et al.: Photosystem I light-harvesting complex Lhca4 adopts multiple conformations: Red forms and excited-state quenching are mutually exclusive.–BBA-Bioenergetics 1797: 501–508, 2010.

    Article  PubMed  CAS  Google Scholar 

  • Rizzo F., Zucchelli G., Jennings R. et al.: Wavelength dependence of the fluorescence emission under conditions of open and closed Photosystem II reaction centres in the green alga Chlorella sorokiniana.–BBA-Bioenergetics 1837: 726–733, 20

    Article  PubMed  CAS  Google Scholar 

  • Ruban A.V., Horton P.: Spectroscopy of nonphotochemical and photochemical quenching of chlorophyll fluorescence in leaves; evidence for a role of the light-harvesting complex of photosystem-ii in the regulation of energy dissipation.–Photosynth. Res. 40: 181–190, 1994.

    Article  PubMed  CAS  Google Scholar 

  • Ruban A.V., Johnson M.P., Duffy C.D.P.: The photoprotective molecular switch in the photosystem II antenna.–BBABioenergetics 1817: 167–181, 2012.

    Article  CAS  Google Scholar 

  • Ruban A.V., Lavaud J., Rousseau B. et al.: The super-excess energy dissipation in diatom algae: comparative analysis with higher plants.–Photosynth. Res. 82: 165–175, 2004.

    Article  PubMed  CAS  Google Scholar 

  • Santabarbara S., Jennings R.C.: The size of the population of weakly coupled chlorophyll pigments involved in thylakoid photoinhibition determined by steady-state fluorescence spectroscopy.–BBA-Bioenergetics 1709: 138–149, 2005.

    Article  PubMed  CAS  Google Scholar 

  • Schreiber U.: Pulse-Amplitude-Modulation (PAM) fluorometry and saturation pulse method: An overview.–In: Papageorgiou G.C. and {ieGovindjee (ed.): Chlorophyll a Fluorescence: A Signature of Photosynthesis. Pp. 279–319. Springer, Dordrecht 2004.

    Chapter  Google Scholar 

  • Vass I.: Role of charge recombination processes in photodamage and photoprotection of the photosystem II complex.–Physiol. Plantarum 142: 6–16, 2011.

    Article  CAS  Google Scholar 

  • Xu P.Q., Tian L.J., Kloz M. et al.: Molecular insights into zeaxanthin-dependent quenching in higher plants.–Sci. Rep. 5: 13679, 2015.

    Article  PubMed  PubMed Central  Google Scholar 

  • Zimorski V., Ku C., Martin W.F. et al.: Endosymbiotic theory for organelle origins.–Curr. Opin. Microbiol. 22: 38–48, 2014.

    Article  PubMed  CAS  Google Scholar 

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Authors and Affiliations

  1. Institute of Microbiology, Czech Academy of Sciences, Třeboň, Czech Republic

    R. Kaňa

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  1. R. Kaňa
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Correspondence to R. Kaňa.

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Acknowledgement: This research was supported by the Czech Science Foundation (project GACR 16–10088S) and by institutional projects Algatech Plus (MSMT LO1416) by the Czech Ministry of Education, Youth and Sport. I’m thankful to Ondřej Prášil for jointly developing the Spectrally Resolved Fluorescence Induction (SRFI) method described previously (Kaňa et al. 2009a, 2012a), and to Govindjee for long-term cooperation and useful discussion of the topic. I also highly appreciate technical assistance, software development and various methodical and physiological measurements that have been done by several members of our lab (namely Jaroslav Krafl, Barbora Šedivá, Jiří Šetlík, Eva Kotabová, and Gabor Steinbach) that allowed continual improvement of the SRFI method and its applicability for different organisms/questions. I would like to thank Erica Belgio for critical reading of the manuscript.

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Kaňa, R. Application of spectrally resolved fluorescence induction to study light-induced nonphotochemical quenching in algae. Photosynthetica 56, 132–138 (2018). https://doi.org/10.1007/s11099-018-0780-1

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