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Effect of dichromate on photosystem II activity in xanthophyll-deficient mutants of Chlamydomonas reinhardtii

Photosynthesis Research volume 95, pages 45–53 (2008)Cite this article

Abstract

The photosystem II activity and energy dissipation was investigated when algal Chlamydomonas reinhardtii genotypes were exposed to dichromate toxicity effect. The exposure during 24 h to dichromate effect of two C. reinhardtii mutants having non-functional xanthophylls cycle, as npq1 zeaxanthin deficient and npq2 zeaxanthin accumulating, induced inhibition of PSII electron transport. After dichromate-induced toxicity, PSII functions of C. reinhardtii mutants were investigated under different light intensities. To determine dichromate toxicity and light intensity effect on PSII functional properties we investigated the change of energy dissipation via PSII electron transport, non-photochemical regulated and non-regulated energy dissipation according to Kramer et al. (Photosynth Res 79:209–218, 2004). We showed the dependency between dichromate toxicity and light-induced photoinhibition in algae deficient in xanthophyll cycle. When algal mutants missing xanthophylls cycle were exposed to dichromate toxicity and to high light intensity energy dissipation via non-regulated mechanism takes the most important pathway reaching the value of 80%. Therefore, the mutants npq1 and npq2 having non-functional xanthophylls cycle were more sensitive to dichromate toxic effects.

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Abbreviations

D1:

A core protein of the photosystem II reaction center

DCPIP:

2,6-dichlorophenol indophenol

DPC:

Diphenyl-carbazide

FO and FO′:

Fluorescence yields when all reaction centers of PSII are oxidized under dark and light adapted state, respectively

FM and FM′:

Maximal fluorescence yields in dark and light adapted state, respectively

F:

Fluorescence yield at any time of induction by an actinic radiation

LHC:

Light harvesting complexes

NPQ:

Fluorescence non-photochemical quenching

PSII:

Photosystem II

qL:

Fraction of open PSII reaction center participating in electron transport

qP:

Fluorescence photochemical quenching

QA and QB :

PSII primary and secondary electron acceptors, respectively

ROS:

Reactive oxygen species

Y(II):

Effective quantum yield of PSII photochemistry

Y(NPQ):

Quantum yield of regulated energy dissipation of PSII

Y(NO):

Quantum yield of non-regulated energy dissipation of PSII

References

  • Ait Ali N, Dewez D, Didur O, Popovic R (2006) Inhibition of photosystem II photochemistry by Cr is caused by the alteration of D1 protein and oxygen evolving complex. Photosynth Res 89:81–87

    Article  Google Scholar 

  • Appenroth KJ, Stöckel J, Srivastava A, Strasser RJ (2001) Multiple effects of chromate on the photosynthetic apparatus of Spirodela polyrhiza as probed by OJIP chlorophyll a fluorescence measurements. Environ Pollut 115:49–64

    Article  PubMed  CAS  Google Scholar 

  • Appenroth KJ, Keresztes A, Sarvari E, Jaglarz A, Fischer W (2003) Multiple effects of chromate on Spirodela polyrhiza: electron microscopy and biochemical investigations. Plant Biol 5:315–323

    Article  CAS  Google Scholar 

  • Bertrand M, Schoefs B, Siffel P, Rohacek K, Molnar I (2001) Cadmium inhibits epoxidation of diatoxanthin to diadinoxanthin in the xanthophyll cycle of the marine diatom Phaeodactylum tricornutum. FEBS Lett 508:153–156

    Article  PubMed  CAS  Google Scholar 

  • Demmig-Adams B, Gilmore AM, Adams WW (1996) In vivo functions of carotenoids in higher plants. FASEB J 10:403–412

    PubMed  CAS  Google Scholar 

  • Dewez D, Geoffrey L, Vernet G, Popovic R (2005) Determination of photosynthetic and enzymatic biomarkers sensitivity used to evaluate toxic effects of copper ions and fludioxonil in alga Scenedesmus obliquus. Aquat Toxicol 74:150–159

    Article  PubMed  CAS  Google Scholar 

  • Garcia-Mendoza E, Matthijs HC, Schubert H, Mur LR (2002) Non-photochemical quenching of chlorophyll fluorescence in Chlorella fusca acclimated to constant and dynamic light conditions. Photosynth Res 74:303–315

    Article  PubMed  CAS  Google Scholar 

  • 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 990:87–92

    CAS  Google Scholar 

  • Govindjee, Seufferheld M (2002) Non-photochemical quenching of chlorophyll a fluorescence: early history and characterization of two xanthophylls-cycle mutants of Chlamydomonas reinhardtii. Func Plant Biol 29:1141–1155

    Article  CAS  Google Scholar 

  • Harris EH (1989) The Chlamydomonas sourcebook: a comprehensive guide to biology and laboratory use. Academic Press, San Diego, CA

    Google Scholar 

  • Horton P, Ruban AV, Walters RG (1994) Regulation of light harvesting in green plants. Plant Physiol 106:415–420

    PubMed  CAS  Google Scholar 

  • Hörcsik ZT, Kovacs L, Laposi R, Meszaros I, Lakatos G, Garab G (2007) Effect of chromium on photosystem 2 in the unicellular green alga, Chlorella pyrenoidosa. Photosynthetica 45:65–69

    Article  Google Scholar 

  • Jahns P, Depka B, Trebst A (2000) Xanthophyll cycle mutans from Chlamydomonas reinhardtii indicate a role for zeaxanthin in the D1 protein turnover. Plant Physiol Biochem 38:371–376

    Article  CAS  Google Scholar 

  • Kitao M, Utsugi H, Kuramoto S, Tabuchi R, Fujimoto K, Lihpai S (2003) Light-dependent photosynthetic characteristics indicated by chlorophyll fluorescence in five mangrove species native to Pohnpei Island, Micronesia. Physiol Plant 117:376–382

    Article  PubMed  CAS  Google Scholar 

  • Kramer DM, Johnson G, Kiirats O, Edwards GE (2004) New fluorescence parameters for the determination of QA redox state and excitation energy fluxes. Photosynth Res 79:209–218

    Article  PubMed  CAS  Google Scholar 

  • Krause GH, Jahns P (2004) Non-photochemical energy dissipation determined by chlorophyll fluorescence quenching: characterization and function. In: Papageorgious GC, Govindjee (eds) chlorophyll a fluorescence: a signature of photosynthesis. Springer, The Netherlands, pp 463–495

    Google Scholar 

  • Lichtenthaler HK (1987) Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. In: Packer L, Douce R (eds) Methods in enzymology, vol 148. Academic Press, London, pp 350–382

    Google Scholar 

  • Lupinková L, Komenda J (2004) Oxidative modifications of the photosystem II D1 protein by reactive oxygen species: from isolated protein to Cyanobacterial cells. Photochem Photobiol 79:152–162

    Article  PubMed  Google Scholar 

  • Mallick N, Mohn FH (2003) Use of chlorophyll fluorescence in metal-stress research: a case study with the green microalga Scenedesmus. Ecotox Environ Saf 55:64–69

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Melis A (1999) Photosystem II damage and repair cycle in chloroplasts: what modulates the rate of photodamage? Trends Plant Sci 4:130–135

    Article  PubMed  Google Scholar 

  • Müller P, Li XP, Niyogi KK (2001) Non-photochemical quenching: a response to excess light energy. Plant Physiol 125:1558–1566

    Article  PubMed  Google Scholar 

  • Mysliwa-Kurdziel B, Strzalka K (2005) Influence of Cd(II), Cr(VI) and Fe(III) on early steps of deetiolation process in wheat: fluorescence spectral changes of protochlorophyllide and newly formed chlorophyllide. Agric Ecosyst Environ 106:199–207

    Article  CAS  Google Scholar 

  • Nishiyama Y, Allakhverdiev SI, Yamamoto H, Hayashi H, Murata N (2004) Singlet oxygen inhibits the repair of photosystem II by suppressing the translation elongation of the D1 protein in Synechocystis sp. PCC 6803. Biochemistry 43:11321–11330

    Article  PubMed  CAS  Google Scholar 

  • Niyogi KK, Bjorkman O, Grossman AR (1997) Chlamydomonas xanthophylls cycle mutants identified by video imaging of chlorophyll fluorescence quenching. Plant Cell 8:1369–1380

    Article  Google Scholar 

  • Oquist G, Huner NPA (1993) Cold-hardening-induced resistance to photoinhibition of photosynthesis in winter rye dependent upon an increased capacity for photosynthesis. Planta 189:150–156

    Article  Google Scholar 

  • Oxborough K, Baker NR (1997) Resolving chlorophyll a fluorescence images of photosynthetic efficiency into photochemical and non-photochemical components-calculation of qP and FV′/F′m without measuring FO′. Photosynth Res 54:135–142

    Article  CAS  Google Scholar 

  • Pagliano C, Raviolo M, Vecchia FD, Gabbrielli R, Gonnelli C, Rascio N, Barbato R, La Rocca N (2006) Evidence for PSII donor-side damage and photoinhibition induced by cadmium treatment on rice (Oryza sativa L.). J Photochem Photobiol 84:70–78

    Article  CAS  Google Scholar 

  • Pätsikkä E, Aro E, Tyystjärvi E (1998) Increase in the quantum yield photoinhibition contributes to copper toxicity in vivo. Plant Physiol 117:619–627

    Article  PubMed  Google Scholar 

  • Pospisil P (1997) Mechanisms of non-photochemical chlorophyll fluorescence quenching in higher plants. Photosynthetica 34:343–355

    Article  CAS  Google Scholar 

  • Prasad SM, Singh JB, Rai LC, Kumar HD (1991) Metal-induced inhibition of photosynthetic electron transport chain of the cyanobacterium Nostoc muscorum. FEMS Microbiol Lett 82:95–100

    Article  CAS  Google Scholar 

  • Rohacek K (2002) Chlorophyll fluorescence parameters: the definitions, photosynthetic meaning, and mutual relationships. Photosynthetica 40:13–29

    Article  CAS  Google Scholar 

  • Schreiber U, Schliwa U, Bilger W (1986) Continuous recording of photochemical and non-photochemical chloropyll fluorescence quenching with a new type of modulation fluorometer. Photosynth Res 10:51–62

    Article  CAS  Google Scholar 

  • Serôdio J, Cruz S, Vieira S, Brotas V (2005) Non-photochemical quenching of chlorophyll fluorescence and operation of the xanthophyll cycle in estuarine microphytobenthos. J Exp Marine Biol Ecol 326:157–169

    Article  Google Scholar 

  • Singh PK, Tewari RK (2003) Cadmium toxicity induced changes in plant water relations and oxidative metabolism of Brassica juncea L. plants. J Environ Biol 24:107–112

    PubMed  CAS  Google Scholar 

  • Susplugas S, Srivastava A, Strasser RJ (2000) Changes in the photosynthetic activities during several stages of vegetative growth of Spirodela polyrhiza: effect of dichromate. J Plant Physiol 157:503–512

    CAS  Google Scholar 

  • White AJ, Critchley C (1999) Rapid light curves: a new fluorescence method to assess the state of the photosynthetic apparatus. Photosynth Res 59:63–72

    Article  CAS  Google Scholar 

  • Wong PK, Chang L (1991) Effect of copper, chromium and nickel on growth, photosynthesis and chlorophyll a synthesis of chlorella pyrenoidosa 251. Environ Pollut 72:127–139

    Article  PubMed  CAS  Google Scholar 

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Acknowledgements

This research was supported by the Natural Science and Engineering Council of Canada (NSERC) through Grant GP0093404 awarded to R. Popovic.

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Authors and Affiliations

  1. Department of Chemistry, Environmental Toxicology Research Center, TOXEN, University of Quebec in Montreal, 2101, Jeanne-Mance, Montreal, QC, Canada, H2X 2J6

    Nadia Ait Ali, Olivier Didur, François Perreault & Radovan Popovic

  2. Department of Biological Sciences – TOXEN, Canadian Research Chair on Ecotoxicology of Aquatic Microorganisms, University of Quebec in Montreal, C.P. 8888, Succ. Centre-ville, Montreal, QC, Canada, H3C 3P8

    Philippe Juneau

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  1. Nadia Ait Ali
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  2. Philippe Juneau
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  3. Olivier Didur
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  4. François Perreault
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  5. Radovan Popovic
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Correspondence to Radovan Popovic.

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Ait Ali, N., Juneau, P., Didur, O. et al. Effect of dichromate on photosystem II activity in xanthophyll-deficient mutants of Chlamydomonas reinhardtii . Photosynth Res 95, 45–53 (2008). https://doi.org/10.1007/s11120-007-9227-4

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  • DOI: https://doi.org/10.1007/s11120-007-9227-4

Keywords

  • Photosystem II energy dissipation
  • Xanthophyll cycle
  • Zeaxanthin
  • Dichromate
  • Chlamydomonas reinhardtii
  • MAXI-IMAGING-PAM fluorometry