Skip to main content
SpringerLink
Log in

High Light Acclimation in Green Microalgae

  • Chapter
  • First Online:
Non-Photochemical Quenching and Energy Dissipation in Plants, Algae and Cyanobacteria

Part of the book series: Advances in Photosynthesis and Respiration ((AIPH,volume 40))

Summary

Absorption of light in excess of the capacity for photosynthetic electron transport can be detrimental for photosynthetic organisms. Mechanisms exist to protect chloroplasts from damage, which are in general associated with photosystem II and collectively assessed via non-photochemical quenching (NPQ) of chlorophyll fluorescence. Non-photochemical quenching comprises several components, including (1) qE (high-energy state quenching, as the rapid component of NPQ) as a measure of thermal dissipation linked to the development of a low pH in the thylakoid lumen and possibly (2) qT (state transition-dependent quenching, as the slower component of NPQ) as a measure of antenna size reduction involving phosphorylation and migration of antenna proteins from PS II to PS I. The relative amplitude and efficiency of these processes is extremely variable in different photosynthetic organisms (the relative amplitude of the latter is especially more prominent in microalgae than vascular plants), likely reflecting the different molecular machineries and/or regulation of the effectors for the processes underlying qE and state transitions in these organisms. The present review focuses on NPQ in green microalgae and summarizes changes in the latter two NPQ components in photosynthetic microalgae (in particular green algae including Ostreococcus, Chlamydomonas, Dunaliella, and Chlorella). We also relate these changes to possible differences between their molecular machineries, which reflect specific responses of each organism to the constraints existing in its environmental niche. Moreover, alternative photoprotective responses based on changes in the electron flow modes/efficiencies are also presented along with an interpretation as to how these mechanisms can provide a benefit for specific photosynthetic organisms.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 229.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 299.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 299.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Abbreviations

A –:

Antheraxanthin;

bf –:

The cytochrome b 6 f complex;

CEF –:

Cyclic electron flow;

Chl –:

Chlorophyll;

CP26 –:

26 kD minor monomeric light-harvesting complex II protein;

CP29 –:

29 kD minor monomeric light-harvesting complex II protein;

CP43 –:

43 kD chlorophyll-binding inner antenna protein;

CP47 –:

47 kD chlorophyll-binding inner antenna protein;

Cys –:

The amino acid cysteine;

D1 –:

D1 subunit of photosystem II;

D2 –:

D2 subunit of photosystem II;

DBMIB –:

2,5-dibromo-3-methyl-6-isopropylbenzoquinone;

DCCD –:

Dicyclohexylcarbodiimide;

DCMU –:

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

Fd –:

Ferredoxin;

Fm – :

Maximum fluorescence;

FNR –:

Ferredoxin-NADP+ oxidoreductase;

His –:

The amino acid histidine;

HQNO –:

2-heptyl-4-hydroxyquinoline-N-oxide;

LEF –:

Linear electron flow;

LHC –:

Light-harvesting complex;

Lhcb1 –:

Light-harvesting complex II protein type I;

Lhcb2 –:

Light-harvesting complex II protein type II;

LHCBM –:

Light-harvesting complex II major protein;

LHCSR –:

Light harvesting complex stress related protein;

NPQ –:

Non-photochemical quenching of chlorophyll fluorescence;

p – :

PS II connectivity parameter;

P700 –:

Reaction center chlorophyll of photosystem I;

Pc –:

Plastocyanin;

pK –:

Negative logarithm of an equilibrium constant;

PP2C –:

Protein phosphatase type 2C;

PPH1 –:

Phosphatase 1;

PQ –:

Plastoquinone;

PQH2 – :

Plastoquinol;

PS –:

Photosystem;

PsaA –:

PsaA subunit of photosystem I;

PsaH –:

PsaH subunit of photosystem I;

PsaI –:

PsaI subunit of photosystem I;

PsaK –:

PsaK subunit of photosystem I;

PsaL –:

PsaL subunit of photosystem I;

PsaO –:

PsaO subunit of photosystem I;

PsbS –:

PsbS subunit of photosystem II;

PTOX –:

Plastoquinone terminal oxidase;

QA – :

First quinone acceptor in the PS II reaction center;

qE –:

ΔpH-dependent component of non-photochemical quenching;

qI –:

Photoinhibition-dependent component of non-photochemical quenching;

qT –:

State transition-dependent component of non-photochemical quenching;

RNAi –:

Ribonucleic acid interference;

Ser –:

The amino acid serine;

TAP38 –:

Thylakoid-associated phosphatase 38;

Thr –:

The amino acid threonine;

V –:

Violaxanthin;

VHLR – :

Very high light resistant nuclear mutants of Chlamydomonas reinhardtii;

Z –:

Zeaxanthin

References

  • Adams WW III, Demmig-Adams B, Verhoeven AS, Barker DH (1995) ‘Photoinhibition’ during winter stress: involvement of sustained xanthophyll cycle-dependent energy dissipation. Aust J Plant Physiol 22:261–276

    CAS  Google Scholar 

  • Alboresi A, Gerotto C, Giacometti GM, Bassi R, Morosinotto T (2010) Physcomitrella patens mutants affected on heat dissipation clarify the evolution of photoprotection mechanisms upon land colonization. Proc Natl Acad Sci USA 107:11128–11133

    CAS  PubMed Central  PubMed  Google Scholar 

  • Allen JF (1992) Protein phosphorylation in regulation of photosynthesis. Biochim Biophys Acta 1098:275–335

    CAS  PubMed  Google Scholar 

  • Allen JF, Bennett J (1981) Photosynthetic protein phosphorylation in intact chloroplasts: inhibition by DCMU and by the onset of CO2 fixation. FEBS Lett 123:67–70

    CAS  Google Scholar 

  • Allen JF, Forsberg J (2001) Molecular recognition in thylakoid structure and function. Trends Plant Sci 6:317–326

    CAS  PubMed  Google Scholar 

  • Allen JF, Horton P (1981) Chloroplast protein phosphorylation and chlorophyll fluorescence quenching. Activation by tetramethyl-p-hydroquinone, an electron donor to plastoquinone. Biochim Biophys Acta 638:290–295

    CAS  Google Scholar 

  • Allen JF, Bennett J, Steinback KE, Arntzen CJ (1981) Chloroplast protein phosphorylation couples plastoquinone redox state to distribution of excitation energy between photosystems. Nature 291:25–29

    CAS  Google Scholar 

  • Allorent G, Tokutsu R, Roach T, Peers G, Cardol P, Girard-Bascou J, Seigneurin-Berny D, Petroutsos D, Kuntz M, Breyton C, Franck F, Wollman FA, Niyogi KK, Krieger-Liszkay A, Minagawa J, Finazzi G (2013) A dual strategy to cope with high light in Chlamydomonas reinhardtii. Plant Cell 25:545–557

    CAS  PubMed Central  PubMed  Google Scholar 

  • Amunts A, Toporik H, Borovikova A, Nelson N (2010) Structure determination and improved model of plant photosystem I. J Biol Chem 285:3478–3486

    CAS  PubMed Central  PubMed  Google Scholar 

  • Andersson B, Anderson JM (1980) Lateral heterogeneity in the distribution of chlorophyll-protein complexes of the thylakoid membranes of spinach chloroplasts. Biochim Biophys Acta 593:427–440

    CAS  PubMed  Google Scholar 

  • Andersson B, Åkerlund H-E, Jergil B, Larsson C (1982) Differential phosphorylation of the light-harvesting chlorophyll-protein complex in appressed and non-appressed regions of the thylakoid membrane. FEBS Lett 149:181–185

    CAS  Google Scholar 

  • Aro E-M, Ohad I (2003) Redox regulation of thylakoid protein phosphorylation. Antioxid Redox Signal 5:55–67

    CAS  PubMed  Google Scholar 

  • Aro E-M, Virgin I, Andersson B (1993) Photoinhibition of photosystem II. Inactivation, protein damage and turnover. Biochim Biophys Acta 1143:113–134

    CAS  PubMed  Google Scholar 

  • Bailey S, Melis A, Mackey KR, Cardol P, Finazzi G, van Dijken G, Berg GM, Arrigo K, Shrager J, Grossman AR (2008) Alternative photosynthetic electron flow to oxygen in marine Synechococcus. Biochim Biophys Acta 1777:269–276

    CAS  PubMed  Google Scholar 

  • Bailleul B, Rogato A, de Martino A, Coesel S, Cardol P, Bowler C, Falciatore A, Finazzi G (2010) 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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Barber J, Andersson B (1992) Too much of a good thing: light can be bad for photosynthesis. Trends Biochem Sci 17:61–66

    CAS  PubMed  Google Scholar 

  • Bassi R, Rigoni F, Barbato R, Giacometti GM (1988) Light-harvesting chlorophyll a/b protein (LHCII) populations in phosphorylated membranes. Biochim Biophys Acta 936:29–38

    CAS  Google Scholar 

  • Bellafiore S, Barneche F, Peltier G, Rochaix J-D (2005) State transitions and light adaptation require chloroplast thylakoid protein kinase STN7. Nature 433:892–895

    CAS  PubMed  Google Scholar 

  • Bennett J (1977) Phosphorylation of chloroplast membrane polypeptides. Nature 269:344–346

    CAS  Google Scholar 

  • Bennett J (1979) Chloroplast phosphoproteins. The protein kinase of thylakoid membranes is light-dependent. FEBS Lett 103:342–344

    CAS  PubMed  Google Scholar 

  • Bennett J, Steinback KE, Arntzen CJ (1980) Chloroplast phosphoproteins: regulation of excitation energy transfer by phosphorylation of thylakoid membrane polypeptides. Proc Natl Acad Sci USA 77:5253–5257

    CAS  PubMed Central  PubMed  Google Scholar 

  • Bennett J, Shaw EK, Michel H (1988) Cytochrome b 6 f complex is required for phosphorylation of light-harvesting chlorophyll a/b complex II in chloroplast photosynthetic membranes. Eur J Biochem 171:95–100

    CAS  PubMed  Google Scholar 

  • Ben-Shem A, Frolow F, Nelson N (2003) Crystal structure of plant photosystem I. Nature 426:630–635

    CAS  PubMed  Google Scholar 

  • Berry S, Rumberg B (1999) Proton to electron stoichiometry in electron transport of spinach thylakoids. Biochim Biophys Acta 1410:248–261

    CAS  PubMed  Google Scholar 

  • Bhalla P, Bennett J (1987) Chloroplast phosphoproteins: phosphorylation of a 12-kDa stromal protein by the redox-controlled kinase of thylakoid membranes. Arch Biochem Biophys 252:97–104

    CAS  PubMed  Google Scholar 

  • Bilger W, Björkman O (1990) Role of the xanthophyll cycle in photoprotection elucidated by measurements of light-induced absorbance changes, fluorescence and photosynthesis in leaves of Hedera canariensis. Photosynth Res 25:173–185

    CAS  PubMed  Google Scholar 

  • Black MT, Lee P, Horton P (1986) Changes in topography and function of thylakoid membranes following membrane protein phosphorylation. Planta 168:330–336

    CAS  PubMed  Google Scholar 

  • Bonaventura C, Myers J (1969) Fluorescence and oxygen evolution from Chlorella pyrenoidosa. Biochim Biophys Acta 189:366–383

    CAS  PubMed  Google Scholar 

  • Bonente G, Howes BD, Caffarri S, Smulevich G, Bassi R (2008) Interactions between the photosystem II subunit PsbS and xanthophylls studied in vivo and in vitro. J Biol Chem 283:8434–8445

    CAS  PubMed Central  PubMed  Google Scholar 

  • Bonente G, Ballottari M, Truong TB, Morosinotto T, Ahn TK, Fleming GR, Niyogi KK, Bassi R (2011) Analysis of LhcSR3, a protein essential for feedback de-excitation in the green alga Chlamydomonas reinhardtii. PLoS Biol 9:e1000577

    CAS  PubMed Central  PubMed  Google Scholar 

  • Bonente G, Pippa S, Castellano S, Bassi R, Ballottari M (2012) Acclimation of Chlamydomonas reinhardtii to different growth irradiances. J Biol Chem 287:5833–5847

    CAS  PubMed Central  PubMed  Google Scholar 

  • Breitholtz HL, Srivastava R, Tyystjärvi E, Rintamäki E (2005) LHC II protein phosphorylation in leaves of Arabidopsis thaliana mutants deficient in non-photochemical quenching. Photosynth Res 84:217–223

    CAS  PubMed  Google Scholar 

  • Briantais JM, Vernotte C, Picaud M, Krause GH (1979) A quantitative study of the slow decline of chlorophyll a fluorescence in isolated chloroplasts. Biochim Biophys Acta 548:128–138

    CAS  PubMed  Google Scholar 

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

    Google Scholar 

  • Cardol P, Bailleul B, Rappaport F, Derelle E, Beal D, Breyton C, Bailey S, Wollman FA, Grossman A, Moreau H, Finazzi G (2008) An original adaptation of photosynthesis in the marine green alga Ostreococcus. Proc Natl Acad Sci USA 105:7881–7886

    CAS  PubMed Central  PubMed  Google Scholar 

  • Cardol P, Forti G, Finazzi G (2011) Regulation of electron transport in microalgae. Biochim Biophys Acta 1807:912–918

    CAS  PubMed  Google Scholar 

  • Carol P, Kuntz M (2001) A plastid terminal oxidase comes to light: implications for carotenoid biosynthesis and chlororespiration. Trends Plant Sci 6:31–36

    CAS  PubMed  Google Scholar 

  • Carol P, Stevenson D, Bisanz C, Breitenbach J, Sandmann G, Mache R, Coupland G, Kuntz M (1999) Mutations in the Arabidopsis gene IMMUTANS cause a variegated phenotype by inactivating a chloroplast terminal oxidase associated with phytoene desaturation. Plant Cell 11:57–68

    CAS  PubMed Central  PubMed  Google Scholar 

  • Chow WS, Telfer A, Chapman DJ, Barber J (1981) State 1-state 2 transition in leaves and its association with ATP-induced chlorophyll fluorescence quenching. Biochim Biophys Acta 638:60–68

    CAS  Google Scholar 

  • Cleland RE, Demmig-Adams B, Adams WW III, Winter K (1990) Phosphorylation state of the light-harvesting chlorophyll-protein complex of photosystem II and fluorescence characteristics in Monstera deliciosa Liebm. and Glycine max (L.) Merrill in response to light. Aust J Plant Physiol 17:589–599

    CAS  Google Scholar 

  • Coughlan SJ, Hind G (1986) Protein kinases of the thylakoid membrane. J Biol Chem 261:14062–14068

    CAS  PubMed  Google Scholar 

  • Coughlan S, Hind G (1987) Phosphorylation of thylakoid proteins by a purified kinase. J Biol Chem 262:8402–8408

    CAS  PubMed  Google Scholar 

  • Dall’Osto L, Caffarri S, Bassi R (2005) A mechanism of nonphotochemical energy dissipation, independent from PsbS, revealed by a conformational change in the antenna protein CP26. Plant Cell 17:1217–1232

    PubMed Central  PubMed  Google Scholar 

  • Davies JP, Grossman AR (1998) Responses to deficiencies in micronutrients. In: Rochaix JD, Goldschmidt-Clermont M, Merchant S (eds) The Molecular Biology of Chloroplasts and Mitochondria in Chlamydomonas. Kluwer Academic Publishers, Dordrecht, pp 613–635

    Google Scholar 

  • Dekker JP, Boekema EJ (2005) Supramolecular organization of thylakoid membrane proteins in green plants. Biochim Biophys Acta 1706:12–39

    CAS  PubMed  Google Scholar 

  • Delosme R, Olive J, Wollman F-A (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 1273:150–158

    Google Scholar 

  • Demmig-Adams B, Adams WW III (1990) The carotenoid zeaxanthin and ‘high-energy-state quenching’ of chlorophyll fluorescence. Photosynth Res 25:187–197

    CAS  PubMed  Google Scholar 

  • Demmig-Adams B, Ebbert V, Mellman DL, Mueh KE, Schaffer L, Funk C, Zarter CR, Adamska I, Jansson S, Adams WW III (2006) Modulation of PsbS and flexible vs sustained energy dissipation by light environment in different species. Physiol Plant 127:670–680

    CAS  Google Scholar 

  • Depège N, Bellafiore S, Rochaix J-D (2003) Role of chloroplast protein kinase Stt7 in LHCII phosphorylation and state transition in Chlamydomonas. Science 299:1572–1575

    PubMed  Google Scholar 

  • Drop B, Webber-Birungi M, Fusetti F, Kouril R, Redding KE, Boekema EJ, Croce R (2011) Photosystem I of Chlamydomonas reinhardtii is composed of nine light-harvesting complexes (Lhca) located on one side of the core. J Biol Chem 286:44878–44887

    CAS  PubMed Central  PubMed  Google Scholar 

  • Eberhard S, Finazzi G, Wollman F-A (2008) The dynamics of photosynthesis. Annu Rev Genet 42:463–515

    CAS  PubMed  Google Scholar 

  • Einali A, Shariati M, Sato F, Endo T (2013) Cyclic electron transport around photosystem I and its relationship to non-photochemical quenching in the unicellular green alga Dunaliella salina under nitrogen deficiency. J Plant Res 126:179–186

    CAS  PubMed  Google Scholar 

  • Elrad D, Niyogi KK, Grossman AR (2002) A major light-harvesting polypeptide of photosystem II functions in thermal dissipation. Plant Cell 14:1801–1816

    CAS  PubMed Central  PubMed  Google Scholar 

  • Fadeev VV, Gorbunov MY, Gostev TS (2012) Studying photoprotective processes in the green alga Chlorella pyrenoidosa using nonlinear laser fluorimetry. J Biophoton 5:502–507

    CAS  Google Scholar 

  • Ferrante P, Ballottari M, Bonente G, Giuliano G, Bassi R (2012) LHCBM1 and LHCBM2/7 polypeptides, components of major LHCII complex, have distinct functional roles in photosynthetic antenna system of Chlamydomonas reinhardtii. J Biol Chem 287:16276–16288

    CAS  PubMed Central  PubMed  Google Scholar 

  • Finazzi G (2005) The central role of the green alga Chlamydomonas reinhardtii in revealing the mechanism of state transitions. J Exp Bot 56:383–388

    CAS  PubMed  Google Scholar 

  • Finazzi G, Forti G (2004) Metabolic flexibility of the green alga Chlamydomonas reinhardtii as revealed by the link between state transitions and cyclic electron flow. Photosynth Res 82:327–338

    CAS  PubMed  Google Scholar 

  • Finazzi G, Barbagallo RP, Bergo E, Barbato R, Forti G (2001) Photoinhibition of Chlamydomonas reinhardtii in State 1 and State 2: damages to the photosynthetic apparatus under linear and cyclic electron flow. J Biol Chem 276:22251–22257

    CAS  PubMed  Google Scholar 

  • Finazzi G, Johnson GN, Dall’Osto L, Zito F, Bonente G, Bassi R, Wollman F-A (2006) Nonphotochemical quenching of chlorophyll fluorescence in Chlamydomonas reinhardtii. Biochemistry 45:1490–1498

    CAS  PubMed  Google Scholar 

  • Fleischmann MM, Ravanel S, Delosme R, Olive J, Zito F, Wollman F-A, Rochaix J-D (1999) Isolation and characterization of photoautotrophic mutants of Chlamydomonas reinhardtii deficient in state transition. J Biol Chem 274:30987–30994

    CAS  PubMed  Google Scholar 

  • Förster B, Osmond CB, Boynton JE (2001) Very high light resistant mutants of Chlamydomonas reinhardtii: responses of photosystem II, nonphotochemical quenching and xanthophyll pigments to light and CO2. Photosynth Res 67:5–15

    PubMed  Google Scholar 

  • Gerotto C, Morosinotto T (2013) Evolution of photoprotection mechanisms upon land colonization: evidence of PSBS-dependent NPQ in late Streptophyte algae. Physiol Plant 149:583–598

    CAS  Google Scholar 

  • Goss R, Garab G (2001) Non-photochemical chlorophyll fluorescence quenching and structural rearrangements induced by low pH in intact cells of Chlorella fusca (Chlorophyceae) and Mantoniella squamata (Prasinophyceae). Photosynth Res 67:185–197

    CAS  PubMed  Google Scholar 

  • Goss R, Wilhelm C, Garab G (2000) Organization of the pigment molecules in the chlorophyll a/b/c containing alga Mantoniella squamata (Prasinophyceae) studied by means of absorption, circular and linear dichroism spectroscopy. Biochim Biophys Acta 1457:190–199

    CAS  PubMed  Google Scholar 

  • Goss R, Ann Pinto E, Wilhelm C, Richter M (2006) The importance of a highly active and ΔpH-regulated diatoxanthin epoxidase for the regulation of the PS II antenna function in diadinoxanthin cycle containing algae. J Plant Physiol 163:1008–1021

    CAS  PubMed  Google Scholar 

  • Grieco M, Tikkanen M, Paakkarinen V, Kangasjarvi S, Aro E-M (2012) Steady-state phosphorylation of light-harvesting complex II proteins preserves photosystem I under fluctuating white light. Plant Physiol 160:1896–1910

    CAS  PubMed Central  PubMed  Google Scholar 

  • Haldrup A, Jensen PE, Lunde C, Scheller HV (2001) Balance of power: a view of the mechanism of photosynthetic state transitions. Trends Plant Sci 6:301–305

    CAS  PubMed  Google Scholar 

  • Hammer MF, Markwell J, Sarath G (1997) Purification of a protein phosphatase from chloroplast stroma capable of dephosphorylating the light-harvesting complex-II. Plant Physiol 113:227–233

    CAS  PubMed Central  PubMed  Google Scholar 

  • Hansson M, Vener AV (2003) Identification of three previously unknown in vivo protein phosphorylation sites in thylakoid membranes of Arabidopsis thaliana. Mol Cell Proteomics 2:550–559

    CAS  PubMed  Google Scholar 

  • Harrer R, Bassi R, Testi MG, Schäfer C (1998) Nearest-neighbor analysis of a photosystem II complex from Marchantia polymorpha L. (liverwort), which contains reaction center and antenna proteins. Eur J Biochem 255:196–205

    CAS  PubMed  Google Scholar 

  • Hast T, Follmann H (1996) Identification of two thylakoid-associated phosphatases with protein phosphatase activity in chloroplasts of the soybean (Glycine max). J Photochem Photobiol B 36:313–319

    CAS  Google Scholar 

  • Horton P, Black MT (1981) Light-dependent quenching of chlorophyll fluorescence in pea chloroplasts induced by adenosine 5′-triphosphate. Biochim Biophys Acta 635:53–62

    CAS  PubMed  Google Scholar 

  • Horton P, Ruban AV, Walters RG (1996) Regulation of light harvesting in green plants. Annu Rev Plant Biol Plant Mol Biol 47:655–684

    CAS  Google Scholar 

  • Horton P, Ruban AV, Wentworth M (2000) Allosteric regulation of the light-harvesting system of photosystem II. Philos Trans R Soc Lond B 355:1361–1370

    CAS  Google Scholar 

  • Hou CX, Pursiheimo S, Rintamäki E, Aro E-M (2002) Environmental and metabolic control of LHCII protein phosphorylation: revealing the mechanisms for dual regulation of the LHCII kinase. Plant Cell Environ 25:1515–1525

    CAS  Google Scholar 

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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Ihnken S, Kromkamp JC, Beardall J (2011) Photoacclimation in Dunaliella tertiolecta reveals a unique NPQ pattern upon exposure to irradiance. Photosynth Res 110:123–137

    CAS  PubMed Central  PubMed  Google Scholar 

  • Iwai M, Takahashi Y, Minagawa J (2008) Molecular remodeling of photosystem II during state transitions in Chlamydomonas reinhardtii. Plant Cell 20:2177–2189

    CAS  PubMed Central  PubMed  Google Scholar 

  • Iwai M, Takizawa K, Tokutsu R, Okamuro A, Takahashi Y, Minagawa J (2010a) Isolation of the elusive supercomplex that drives cyclic electron flow in photosynthesis. Nature 464:1210–1213

    CAS  PubMed  Google Scholar 

  • Iwai M, Yokono M, Inada N, Minagawa J (2010b) Live cell imaging of photosystem II antenna dissociation during state transitions. Proc Natl Acad Sci USA 107:2337–2342

    CAS  PubMed Central  PubMed  Google Scholar 

  • Jensen PE, Haldrup A, Zhang S, Scheller HV (2004) The PSI-O subunit of plant photosystem I is involved in balancing the excitation pressure between the two photosystems. J Biol Chem 279:24212–24217

    CAS  PubMed  Google Scholar 

  • Joliot P, Alric J (2013) Inhibition of CO2 fixation by iodoacetamide stimulates cyclic electron flow and non-photochemical quenching upon far-red illumination. Photosynth Res 115:55–63

    CAS  PubMed  Google Scholar 

  • Joliot PA, Finazzi G (2010) Proton equilibration in the chloroplast modulates multiphasic kinetics of nonphotochemical quenching of fluorescence in plants. Proc Natl Acad Sci USA 107:12728–12733

    CAS  PubMed Central  PubMed  Google Scholar 

  • Joliot P, Johnson GN (2011) Regulation of cyclic and linear electron flow in higher plants. Proc Natl Acad Sci USA 108:13317–13322

    CAS  PubMed Central  PubMed  Google Scholar 

  • Joliot A, Joliot P (1964) Étude cinétique de la réaction photochimique libérant l’oxygène au cours de la photosynthèse. C R Hebd Seances Acad Sci 258:4622–4625

    CAS  PubMed  Google Scholar 

  • Kargul J, Turkina MV, Nield J, Benson S, Vener AV, Barber J (2005) Light-harvesting complex II protein CP29 binds to photosystem I of Chlamydomonas reinhardtii under State 2 conditions. FEBS J 272:4797–4806

    CAS  PubMed  Google Scholar 

  • Karpinski S, Gabrys H, Mateo A, Karpinska B, Mullineaux PM (2003) Light perception in plant disease defence signalling. Curr Opin Plant Biol 6:390–396

    CAS  PubMed  Google Scholar 

  • Kouřil R, Zygadlo A, Arteni AA, de Wit CD, Dekker JP, Jensen PE, Scheller HV, Boekema EJ (2005) Structural characterization of a complex of photosystem I and light-harvesting complex II of Arabidopsis thaliana. Biochemistry 44:10935–10940

    PubMed  Google Scholar 

  • Kyle DJ, Staehelin LA, Arntzen CJ (1983) Lateral mobility of the light-harvesting complex in chloroplast membranes controls excitation energy distribution in higher plants. Arch Biochem Biophys 222:527–541

    CAS  PubMed  Google Scholar 

  • Larsson UK, Jergil B, Andersson B (1983) Changes in the lateral distribution of the light-harvesting chlorophyll-a/b-protein complex induced by its phosphorylation. Eur J Biochem 136:25–29

    Google Scholar 

  • Lavaud J, Rousseau B, Etienne A-L (2002a) In diatoms, a transthylakoid proton gradient alone is not sufficient to induce a non-photochemical fluorescence quenching. FEBS Lett 523:163–166

    CAS  PubMed  Google Scholar 

  • Lavaud J, van Gorkom HJ, Etienne A-L (2002b) Photosystem II electron transfer cycle and chlororespiration in planktonic diatoms. Photosynth Res 74:51–59

    CAS  PubMed  Google Scholar 

  • Lemeille S, Willig A, Depège-Fargeix N, Delessert C, Bassi R, Rochaix JD (2009) Analysis of the chloroplast protein kinase Stt7 during state transitions. PLoS Biol 7:e1000045

    PubMed Central  Google Scholar 

  • Li X-P, Björkman O, Shih C, Grossman AR, Rosenquist M, Jansson S, Niyogi KK (2000) A pigment-binding protein essential for regulation of photosynthetic light harvesting. Nature 403:391–395

    CAS  PubMed  Google Scholar 

  • Li X-P, Gilmore AM, Caffarri S, Bassi R, Golan T, Kramer D, Niyogi KK (2004) Regulation of photosynthetic light harvesting involves intrathylakoid lumen pH sensing by the PsbS protein. J Biol Chem 279:22866–22874

    CAS  PubMed  Google Scholar 

  • Lin ZF, Lucero HA, Racker E (1982) Protein kinases from spinach chloroplasts. I Purification and identification of two distinct protein kinases. J Biol Chem 257:12153–12156

    CAS  PubMed  Google Scholar 

  • Lommer M, Specht M, Roy AS, Kraemer L, Andreson R, Gutowska MA, Wolf J, Bergner SV, Schilhabel MB, Klostermeier UC, Beiko RG, Rosenstiel P, Hippler M, Laroche J (2012) Genome and low-iron response of an oceanic diatom adapted to chronic iron limitation. Genome Biol 13:R66

    PubMed Central  PubMed  Google Scholar 

  • Lunde C, Jensen PE, Haldrup A, Knoetzel J, Scheller HV (2000) The PSI-H subunit of photosystem I is essential for state transitions in plant photosynthesis. Nature 408:613–615

    CAS  PubMed  Google Scholar 

  • Mackey KRM, Paytan A, Grossman AR, Bailey S (2008) A photosynthetic strategy for coping in a high-light, low-nutrient environment. Limnol Oceanogr 53:900–913

    CAS  Google Scholar 

  • Michel H, Griffin PR, Shabanowitz J, Hunt DF, Bennett J (1991) Tandem mass spectrometry identifies sites of three post-translational modifications of spinach light-harvesting chlorophyll protein II. Proteolytic cleavage, acetylation, and phosphorylation. J Biol Chem 266:17584–17591

    CAS  PubMed  Google Scholar 

  • Miller R, Wu G, Deshpande RR, Vieler A, Gartner K, Li X, Moellering ER, Zauner S, Cornish AJ, Liu B, Bullard B, Sears BB, Kuo MH, Hegg EL, Shachar-Hill Y, Shiu SH, Benning C (2010) Changes in transcript abundance in Chlamydomonas reinhardtii following nitrogen deprivation predict diversion of metabolism. Plant Physiol 154:1737–1752

    CAS  PubMed Central  PubMed  Google Scholar 

  • Minagawa J (2011) State transitions–the molecular remodeling of photosynthetic supercomplexes that controls energy flow in the chloroplast. Biochim Biophys Acta 1807:897–905

    CAS  PubMed  Google Scholar 

  • Moseley JL, Allinger T, Herzog S, Hoerth P, Wehinger E, Merchant S, Hippler M (2002) Adaptation to Fe-deficiency requires remodeling of the photosynthetic apparatus. EMBO J 21:6709–6720

    CAS  PubMed Central  PubMed  Google Scholar 

  • Murata N (1969) Control of excitation transfer in photosynthesis. I. Light-induced change of chlorophyll a fluoresence in Porphyridium cruentum. Biochim Biophys Acta 172:242–251

    CAS  PubMed  Google Scholar 

  • Nagy G, Ünnep R, Zsiros O, Tokutsu R, Takizawa K, Porcar L, Moyet L, Petroutsos D, Garab G, Finazzi G, Minagawa J (2014) Chloroplast remodeling during state transitions in Chlamydomonas reinhardtii as revealed by non-invasive techniques in vivo. Proc Natl Acad Sci USA 111:5042–5047

    Google Scholar 

  • Naumann B, Busch A, Allmer J, Ostendorf E, Zeller M, Kirchhoff H, Hippler M (2007) Comparative quantitative proteomics to investigate the remodeling of bioenergetic pathways under iron deficiency in Chlamydomonas reinhardtii. Proteomics 7:3964–3979

    CAS  PubMed  Google Scholar 

  • Niyogi KK (1999) Photoprotection revisited: genetic and molecular approaches. Annu Rev Plant Biol Plant Mol Biol 50:333–359

    CAS  Google Scholar 

  • Nymark M, Valle KC, Brembu T, Hancke K, Winge P, Andresen K, Johnsen G, Bones AM (2009) An integrated analysis of molecular acclimation to high light in the marine diatom Phaeodactylum tricornutum. PLoS One 4:e7743

    PubMed Central  PubMed  Google Scholar 

  • Oren A (2005) A hundred years of Dunaliella research: 1905–2005. Saline Syst 1:2

    PubMed Central  PubMed  Google Scholar 

  • Peers G, Truong TB, Ostendorf E, Busch A, Elrad D, Grossman AR, Hippler M, Niyogi KK (2009) An ancient light-harvesting protein is critical for the regulation of algal photosynthesis. Nature 462:518–521

    CAS  PubMed  Google Scholar 

  • Pesaresi P, Lunde C, Jahns P, Tarantino D, Meurer J, Varotto C, Hirtz RD, Soave C, Scheller HV, Salamini F, Leister D (2002) A stable LHCII-PSI aggregate and suppression of photosynthetic state transitions in the psae1-1 mutant of Arabidopsis thaliana. Planta 215:940–948

    CAS  PubMed  Google Scholar 

  • Petroutsos D, Busch A, Janssen I, Trompelt K, Bergner SV, Weinl S, Holtkamp M, Karst U, Kudla J, Hippler M (2011) The chloroplast calcium sensor CAS is required for photoacclimation in Chlamydomonas reinhardtii. Plant Cell 23:2950–2963

    CAS  PubMed Central  PubMed  Google Scholar 

  • Pocock T, Sane PV, Falk S, Huner NPA (2007) Excitation pressure regulates the activation energy for recombination events in the photosystem II reaction centres of Chlamydomonas reinhardtii. Biochem Cell Biol 85:721–729

    CAS  PubMed  Google Scholar 

  • Pribil M, Pesaresi P, Hertle A, Barbato R, Leister D (2010) Role of plastid protein phosphatase TAP38 in LHCII dephosphorylation and thylakoid electron flow. PLoS Biol 8:e1000288

    PubMed Central  PubMed  Google Scholar 

  • Reddy AS, Ali GS, Celesnik H, Day IS (2011) Coping with stresses: roles of calcium- and calcium/calmodulin-regulated gene expression. Plant Cell 23:2010–2032

    CAS  PubMed Central  PubMed  Google Scholar 

  • Rintamäki E, Martinsuo P, Pursiheimo S, Aro E-M (2000) Cooperative regulation of light-harvesting complex II phosphorylation via the plastoquinol and ferredoxin-thioredoxin system in chloroplasts. Proc Natl Acad Sci USA 97:11644–11649

    PubMed Central  PubMed  Google Scholar 

  • Rochaix JD (2007) Role of thylakoid protein kinases in photosynthetic acclimation. FEBS Lett 581:2768–2775

    CAS  PubMed  Google Scholar 

  • Ruban AV, Berera R, Ilioaia C, van Stokkum IH, Kennis JT, Pascal AA, van Amerongen H, Robert B, Horton P, van Grondelle R (2007) Identification of a mechanism of photoprotective energy dissipation in higher plants. Nature 450:575–578

    CAS  PubMed  Google Scholar 

  • Samson G, Bruce D (1995) Complementary changes in absorption cross-sections of photosystems I and II due to phosphorylation and Mg2+-depletion in spinach thylakoids. Biochim Biophys Acta 1232:21–26

    Google Scholar 

  • Seaton GG, Hurry VM, Rohozinski J (1996) Novel amplification of non-photochemical chlorophyll fluorescence quenching following viral infection in Chlorella. FEBS Lett 389:319–323

    CAS  PubMed  Google Scholar 

  • Shapiguzov A, Ingelsson B, Samol I, Andres C, Kessler F, Rochaix JD, Vener AV, Goldschmidt-Clermont M (2010) The PPH1 phosphatase is specifically involved in LHCII dephosphorylation and state transitions in Arabidopsis. Proc Natl Acad Sci USA 107:4782–4787

    CAS  PubMed Central  PubMed  Google Scholar 

  • Silverstein T, Cheng L, Allen JF (1993) Chloroplast thylakoid protein phosphatase reactions are redox-independent and kinetically heterogeneous. FEBS Lett 334:101–105

    CAS  PubMed  Google Scholar 

  • Six C, Worden AZ, Rodriguez F, Moreau H, Partensky F (2005) New insights into the nature and phylogeny of prasinophyte antenna proteins: Ostreococcus tauri, a case study. Mol Biol Evol 22:2217–2230

    CAS  PubMed  Google Scholar 

  • Six C, Finkel ZV, Rodriguez F, Marie D, Partensky F, Campbell DA (2008) Contrasting photoacclimation costs in ecotypes of the marine eukaryotic picoplankter Ostreococcus. Limnol Oceanogr 53:255–265

    CAS  Google Scholar 

  • Six C, Sherrard R, Lionard M, Roy S, Campbell DA (2009) Photosystem II and pigment dynamics among ecotypes of the green alga Ostreococcus. Plant Physiol 151:379–390

    CAS  PubMed Central  PubMed  Google Scholar 

  • Sokolenko A, Fulgosi H, Gal A, Altschmied L, Ohad I, Herrmann RG (1995) The 64 kDa polypeptide of spinach may not be the LHCII kinase, but a lumen-located polyphenol oxidase. FEBS Lett 371:176–180

    CAS  PubMed  Google Scholar 

  • Strzepek RF, Harrison PJ (2004) Photosynthetic architecture differs in coastal and oceanic diatoms. Nature 431:689–692

    CAS  PubMed  Google Scholar 

  • Sun G, Bailey D, Jones MW, Markwell J (1989) Chloroplast thylakoid protein phosphatase is a membrane surface-associated activity. Plant Physiol 89:238–243

    CAS  PubMed Central  PubMed  Google Scholar 

  • Takahashi H, Iwai M, Takahashi Y, Minagawa J (2006) Identification of the mobile light-harvesting complex II polypeptides for state transitions in Chlamydomonas reinhardtii. Proc Natl Acad Sci USA 103:477–482

    CAS  PubMed Central  PubMed  Google Scholar 

  • Takahashi H, Clowez S, Wollman FA, Vallon O, Rappaport F (2013) Cyclic electron flow is redox-controlled but independent of state transition. Nat Commun 4:1954

    PubMed Central  PubMed  Google Scholar 

  • Telfer A, Bottin H, Barber J, Mathis P (1984) The effect of magnesium and phosphorylation of light-harvesting chlorophyll a/b-protein on the yield of P-700-photooxidation in pea chloroplasts. Biochim Biophys Acta 764:324–330

    CAS  Google Scholar 

  • Terashima M, Petroutsos D, Hudig M, Tolstygina I, Trompelt K, Gabelein P, Fufezan C, Kudla J, Weinl S, Finazzi G, Hippler M (2012) Calcium-dependent regulation of cyclic photosynthetic electron transfer by a CAS, ANR1, and PGRL1 complex. Proc Natl Acad Sci USA 109:17717–17722

    CAS  PubMed Central  PubMed  Google Scholar 

  • Thaipratum R, Melis A, Svasti J, Yokthongwattana K (2009) Analysis of non-photochemical energy dissipating processes in wild type Dunaliella salina (green algae) and in zea1, a mutant constitutively accumulating zeaxanthin. J Plant Res 122:465–476

    CAS  PubMed  Google Scholar 

  • Ting CS, Owens TG (1993) Photochemical and nonphotochemical fluorescence quenching processes in the diatom Phaeodactylum tricornutum. Plant Physiol 101:1323–1330

    CAS  PubMed Central  PubMed  Google Scholar 

  • Tokutsu R, Minagawa J (2013) Energy-dissipative supercomplex of photosystem II associated with LHCSR3 in Chlamydomonas reinhardtii. Proc Natl Acad Sci USA 110:10016–10021

    CAS  PubMed Central  PubMed  Google Scholar 

  • Tokutsu R, Iwai M, Minagawa J (2009) CP29, a monomeric light-harvesting complex II protein, is essential for state transitions in Chlamydomonas reinhardtii. J Biol Chem 284:7777–7782

    CAS  PubMed Central  PubMed  Google Scholar 

  • Tokutsu R, Kato N, Bui KH, Ishikawa T, Minagawa J (2012) Revisiting the supramolecular organization of photosystem II in Chlamydomonas reinhardtii. J Biol Chem 287:31574–31581

    CAS  PubMed Central  PubMed  Google Scholar 

  • Trouillard M, Shahbazi M, Moyet L, Rappaport F, Joliot P, Kuntz M, Finazzi G (2012) Kinetic properties and physiological role of the plastoquinone terminal oxidase (PTOX) in a vascular plant. Biochim Biophys Acta 1817:2140–2148

    CAS  PubMed  Google Scholar 

  • Turkina MV, Villarejo A, Vener AV (2004) The transit peptide of CP29 thylakoid protein in Chlamydomonas reinhardtii is not removed but undergoes acetylation and phosphorylation. FEBS Lett 564:104–108

    CAS  PubMed  Google Scholar 

  • Turkina MV, Blanco-Rivero A, Vainonen JP, Vener AV, Villarejo A (2006a) CO2 limitation induces specific redox-dependent protein phosphorylation in Chlamydomonas reinhardtii. Proteomics 6:2693–2704

    CAS  PubMed  Google Scholar 

  • Turkina MV, Kargul J, Blanco-Rivero A, Villarejo A, Barber J, Vener AV (2006b) Environmentally modulated phosphoproteome of photosynthetic membranes in the green alga Chlamydomonas reinhardtii. Mol Cell Proteomics 5:1412–1425

    CAS  PubMed  Google Scholar 

  • Vener AV (2007) Environmentally modulated phosphorylation and dynamics of proteins in photosynthetic membranes. Biochim Biophys Acta 1767:449–457

    CAS  PubMed  Google Scholar 

  • Vener AV, van Kan PJ, Rich PR, Ohad II, Andersson B (1997) Plastoquinol at the quinol oxidation site of reduced cytochrome bf mediates signal transduction between light and protein phosphorylation: thylakoid protein kinase deactivation by a single-turnover flash. Proc Natl Acad Sci USA 94:1585–1590

    CAS  PubMed Central  PubMed  Google Scholar 

  • Vink M, Zer H, Alumot N, Gaathon A, Niyogi KK, Herrmann RG, Andersson B, Ohad I (2004) Light-modulated exposure of the light-harvesting complex II (LHCII) to protein kinase(s) and state transition in Chlamydomonas reinhardtii xanthophyll mutants. Biochemistry 43:7824–7833

    CAS  PubMed  Google Scholar 

  • Wollman F-A (2001) State transitions reveal the dynamics and flexibility of the photosynthetic apparatus. EMBO J 20:3623–3630

    CAS  PubMed Central  PubMed  Google Scholar 

  • Wollman F-A, Lemaire C (1988) Studies on kinase-controlled state transitions in photosystem II and b 6 f mutants from Chlamydomonas reinhardtii which lack quinone-binding proteins. Biochim Biophys Acta 933:85–94

    CAS  Google Scholar 

  • Wraight CA, Crofts AR (1971) Delayed fluorescence and the high-energy state of chloroplasts. Biochim Biophys Acta 19:386–397

    CAS  Google Scholar 

  • Yakushevska AE, Keegstra W, Boekema EJ, Dekker JP, Andersson J, Jansson S, Ruban AV, Horton P (2003) The structure of photosystem II in Arabidopsis: localization of the CP26 and CP29 antenna complexes. Biochemistry 42:608–613

    CAS  PubMed  Google Scholar 

  • Yamamoto HY, Nakayama TO, Chichester CO (1962) Studies on the light and dark interconversions of leaf xanthophylls. Arch Biochem Biophys 97:168–173

    CAS  PubMed  Google Scholar 

  • Zehr JP, Kudela RM (2009) Ocean science. Photosynthesis in the open ocean. Science 326:945–946

    CAS  PubMed  Google Scholar 

  • Zhang S, Scheller HV (2004) Light-harvesting complex II binds to several small subunits of photosystem I. J Biol Chem 279:3180–3187

    CAS  PubMed  Google Scholar 

  • Zhang Z, Shrager J, Jain M, Chang CW, Vallon O, Grossman AR (2004) Insights into the survival of Chlamydomonas reinhardtii during sulfur starvation based on microarray analysis of gene expression. Eukaryot Cell 3:1331–1348

    CAS  PubMed Central  PubMed  Google Scholar 

  • Zhu SH, Green BR (2010) Photoprotection in the diatom Thalassiosira pseudonana: role of LI818-like proteins in response to high light stress. Biochim Biophys Acta 1797:1449–1457

    CAS  PubMed  Google Scholar 

  • Zito F, Finazzi G, Delosme R, Nitschke W, Picot D, Wollman F-A (1999) The Qo site of cytochrome b 6 f complexes controls the activation of the LHCII kinase. EMBO J 18:2961–2969

    CAS  PubMed Central  PubMed  Google Scholar 

Download references

Acknowledgments

GF wishes to thank the financial support from the Agence Nationale de la Recherche, grant “phytadapt” n°NT09_567009, the Labex GRAL (Grenoble Alliance for Integrated Structural Cell Biology) and the Région Rhone Alpes. JM wishes to thank the financial support from the NEXT Program initiated by the Council for Science and Technology Policy Grant (GS026). Support from the Japanese Society of Technology – Conseil National de la Recherche Scientifique cooperative program on Marine Genomics and Marine Biology to GF and JM is also acknowledged.

Author information

Authors and Affiliations

  1. Unité Mixte Recherche 5168, Laboratoire Physiologie Cellulaire et Végétale, Centre National Recherche Scientifique, Grenoble, 38054, France

    Giovanni Finazzi

  2. Commissariat à l’Energie Atomique et Energies Alternatives, l’Institut de Recherches en Technologies et Sciences pour le Vivant, Grenoble, 38054, France

    Giovanni Finazzi

  3. Université Grenoble 1, Grenoble, 38041, France

    Giovanni Finazzi

  4. Institut National Recherche Agronomique, Grenoble, 38054, France

    Giovanni Finazzi

  5. Division of Environmental Photobiology, National Institute for Basic Biology, 38 Nishigonaka, Myodaiji, Okazaki, Aichi, 444-8585, Japan

    Jun Minagawa

Authors
  1. Giovanni Finazzi
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jun Minagawa
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jun Minagawa .

Editor information

Editors and Affiliations

  1. Ecology and Evolutionary Biology, University of Colorado, Boulder, Boulder, Colorado, USA

    Barbara Demmig-Adams

  2. Laboratory of Photosynthetic Membranes Biological Research Center, Institute of Plant Biology Hungarian Academy of Sciences, Szeged, Hungary

    Gyozo Garab

  3. Ecology and Evolutionary Biology, University of Colorado, Boulder, Colorado, USA

    William Adams III

  4. Department of Plant Biology 265 Morrill Hall, MC-116, University of Illinois at Urbana-Champaign, Urbana, Illinois, USA

    Govindjee

Rights and permissions

Reprints and permissions

Copyright information

© 2014 Springer Science+Business Media Dordrecht

About this chapter

Cite this chapter

Finazzi, G., Minagawa, J. (2014). High Light Acclimation in Green Microalgae. In: Demmig-Adams, B., Garab, G., Adams III, W., Govindjee, . (eds) Non-Photochemical Quenching and Energy Dissipation in Plants, Algae and Cyanobacteria. Advances in Photosynthesis and Respiration, vol 40. Springer, Dordrecht. https://doi.org/10.1007/978-94-017-9032-1_21

Download citation

Publish with us

Policies and ethics

Search

Navigation