Skip to main content

Advertisement

SpringerLink
Log in

The supramolecular architecture, function, and regulation of thylakoid membranes in red algae: an overview

  • Review
  • Published:
Photosynthesis Research Aims and scope Submit manuscript

Abstract

Red algae are a group of eukaryotic photosynthetic organisms. Phycobilisomes (PBSs), which are composed of various types of phycobiliproteins and linker polypeptides, are the main light-harvesting antennae in red algae, as in cyanobacteria. Two morphological types of PBSs, hemispherical- and hemidiscoidal-shaped, are found in different red algae species. PBSs harvest solar energy and efficiently transfer it to photosystem II (PS II) and finally to photosystem I (PS I). The PS I of red algae uses light-harvesting complex of PS I (LHC I) as a light-harvesting antennae, which is phylogenetically related to the LHC I found in higher plants. PBSs, PS II, and PS I are all distributed throughout the entire thylakoid membrane, a pattern that is different from the one found in higher plants. Photosynthesis processes, especially those of the light reactions, are carried out by the supramolecular complexes located in/on the thylakoid membranes. Here, the supramolecular architecture, function and regulation of thylakoid membranes in red algal are reviewed.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

Abbreviations

AFM:

Atomic force microscopy

APC:

Allophycocyanin

B-PE:

B-phycoerythrin

Chl:

Chlorophyll

C-PC:

C-phycocyanin

EM:

Electron microscopy

FRAP:

Fluorescence recovery after photobleaching

LHC I:

Light-harvesting complex of photosystem I

LHC II:

Light-harvesting complex of photosystem II

PBP:

Phycobiliprotein

PBS:

Phycobilisome

PC:

Phycocyanin

PCB:

Phycocyanobilin

PE:

Phycoerythrin

PEB:

Phycoerythrobilin

PS I:

Photosystem I

PS II:

Photosystem II

PUB:

Phycourobilin

R-PC:

R-phycocyanin

R-PE:

R-phycoerythrin

References

  • Abe S-i, Murakami A, Ohki K, Aruga Y, Fujita Y (1994) Changes in stoichiometry among PSI, PSII and Cyt b 6-f complexes in response to chromatic light for cell growth observed with the red alga Porphyra yezoensis. Plant Cell Physiol 35:901–906

    Google Scholar 

  • Adachi H, Umena Y, Enami I, Henmi T, Kamiya N, Shen J-R (2009) Towards structural elucidation of eukaryotic photosystem II: purification, crystallization and preliminary X-ray diffraction analysis of photosystem II from a red alga. Biochim Biophys Acta 1787:121–128

    PubMed  CAS  Google Scholar 

  • Adir N, Dines M, Klartag M, McGregor A, Melamed-Frank M (2006) Assembly and disassembly of phycobilisomes. In: Shively JM (ed) Microbiology monographs: inclusions in prokaryotes. Springer, Berlin, pp 47–77

    Google Scholar 

  • Algarra P, Thomas J-C, Mousseau A (1990) Phycobilisome heterogeneity in the red alga Porphyra umbilicalis. Plant Physiol 92:570–576

    PubMed  CAS  Google Scholar 

  • Apt KE, Grossman AR (1993a) Characterization and transcript analysis of the major phycobiliprotein subunit genes from Aglaothamnion neglectum (Rhodophyta). Plant Mol Biol 21:27–38

    PubMed  CAS  Google Scholar 

  • Apt KE, Grossman AR (1993b) Genes encoding phycobilisome linker polypeptides on the plastid genome of Aglaothamnion neglectum (Rhodophyta). Photosynth Res 35:235–245

    CAS  Google Scholar 

  • Apt KE, Hoffman NE, Grossman AR (1993) The gamma subunit of R-phycoerythrin and its possible mode of transport into the plastid of red algae. J Biol Chem 268:16208–16215

    PubMed  CAS  Google Scholar 

  • Apt KE, Collier JL, Grossman AR (1995) Evolution of the phycobiliproteins. J Mol Biol 248:79–96

    PubMed  CAS  Google Scholar 

  • Apt KE, Metzner S, Grossman AR (2001) The γ subunits of phycoerythrin from a red alga: position in phycobilisomes and sequence characterization. J Phycol 37:64–70

    CAS  Google Scholar 

  • Arteni AA, Liu L-N, Aartsma TJ, Zhang Y-Z, Zhou B-C, Boekema EJ (2008) Structure and organization of phycobilisomes on membranes of the red alga Porphyridium cruentum. Photosynth Res 95:169–174

    PubMed  CAS  Google Scholar 

  • Arteni A, Ajlani G, Boekema E (2009) Structural organisation of phycobilisomes from Synechocystis sp. strain PCC6803 and their interaction with the membrane. Biochim Biophys Acta 1787:272–279

    PubMed  CAS  Google Scholar 

  • Bernard C, Etienne A-L, Thomas J-C (1996) Synthesis and binding of phycoerythrin and its associated linkers to the phycobilisome in Rhodella violacea (Rhodophyta): compared effects of high light and translation inhibitors. J Phycol 32:265–271

    CAS  Google Scholar 

  • Bisalputra T, Bailey A (1973) The fine structure of the chloroplast envelope of a red alga, Bangia fusco-purpurea. Protoplasma 76:443–454

    Google Scholar 

  • Bumba L, Havelková-Doušová H, Hušák M, Vácha F (2004) Structural characterization of photosystem II complex from red alga Porphyridium cruentum retaining extrinsic subunits of the oxygen-evolving complex. Eur J Biochem 271:2967–2975

    PubMed  CAS  Google Scholar 

  • Busch A, Nield J, and Hippler M (2010) The composition and structure of photosystem I associated antenna from Cyanidioschyzon merolae. Plant J. doi:10.1111/j.1365-313X.2010.04202.x

  • Chang W-R, Jiang T, Wan Z-L, Zhang J-P, Yang Z-X, Liang D-C (1996) Crystal structure of R-phycoerythrin from Polysiphonia urceolata at 2.8 Ǻ resolution. J Mol Biol 262:721–731

    PubMed  CAS  Google Scholar 

  • Chereskin BM, Clement-Metral JD, Gantt E (1985) Characterization of a purified photosystem II-phycobilisome particle preparation from Porphyridium cruentum. Plant Physiol 77:626–629

    PubMed  CAS  Google Scholar 

  • Clement-Metral JD, Gantt E (1983) Isolation of oxygen-evolving phycobilisome-photosystem II particles from Porphyridium cruentum. FEBS Lett 156:185–188

    CAS  Google Scholar 

  • Clement-Metral JD, Gantt E, Redlinger T (1985) A photosystem II-phycobilisome preparation from the red alga, Porphyridium cruentum: oxygen evolution, ultrastructure, and polypeptide resolution. Arch Biochem Biophys 238:10–17

    PubMed  CAS  Google Scholar 

  • Contreras-Martel C, Martinez-Oyanedel J, Bunster M, Legrand P, Piras C, Vernede X, Fontecilla-Camps JC (2001) Crystallization and 2.2 Ǻ resolution structure of R-phycoerythrin from Gracilaria chilensis: a case of perfect hemihedral twinning. Acta Crystallogr D 57:52–60

    PubMed  CAS  Google Scholar 

  • Contreras-Martel C, Matamala A, Bruna C, Poo-Caamaño G, Almonacid D, Figueroa M, Martínez-Oyanedel J, Bunster M (2007) The structure at 2 Å resolution of phycocyanin from Gracilaria chilensis and the energy transfer network in a PC-PC complex. Biophys Chem 125:388–396

    PubMed  CAS  Google Scholar 

  • Cunningham FX Jr, Dennenberg RJ, Mustardy L, Jursinic PA, Gantt E (1989) Stoichiometry of photosystem I, photosystem II, and phycobilisomes in the red alga Porphyridium cruentum as a function of growth irradiance. Plant Physiol 91:1179–1187

    PubMed  CAS  Google Scholar 

  • Cunningham FX Jr, Dennenberg RJ, Jursinic PA, Gantt E (1990) Growth under red light enhances photosystem II relative to photosystem I and phycobilisomes in the red alga Porphyridium cruentum. Plant Physiol 93:888–895

    PubMed  CAS  Google Scholar 

  • Cunningham FX Jr, Mustárdy L, Gantt E (1991) Irradiance effects on thylakoid membranes of the red alga Porphyridium cruentum. An immunocytochemical study. Plant Cell Physiol 32:419–426

    CAS  Google Scholar 

  • Cunningham FX Jr, Vonshak A, Gantt E (1992) Photoacclimation in the red alga Porphyridium cruentum: changes in photosynthetic enzymes, electron carriers, and light-saturated rate of photosynthesis as a function of irradiance and spectral quality. Plant Physiol 100:1142–1149

    PubMed  CAS  Google Scholar 

  • D’Agnolo E, Rizzo R, Paoletti S, Murano E (1994) R-phycoerythrin from the red alga Gracilaria longa. Phytochem 35:693–696

    Google Scholar 

  • Delphin E, Duval J-C, Kirilovsky D (1995) Comparison of state l-state 2 transitions in the green alga Chlamydomonas reinhardtii and in the red alga Rhodella violacea: effect of kinase and phosphatase inhibitors. Biochim Biophys Acta 1232:91–95

    Google Scholar 

  • Delphin E, Duval J-C, Etienne A-L, Kirilovsky D (1996) State transitions or ΔpH-dependent quenching of photosystem II fluorescence in red algae. Biochemistry 35:9435–9445

    PubMed  CAS  Google Scholar 

  • Delphin E, Duval J-C, Etienne A-L, Kirilovsky D (1998) ΔpH-dependent photosystem II fluorescence quenching induced by saturating, multiturnover pulses in red algae. Plant Physiol 118:103–113

    PubMed  CAS  Google Scholar 

  • Desquilbet TE, Duval J-C, Robert B, Houmard J, Thomas JC (2003) In the unicellular red alga Rhodella violacea iron deficiency induces an accumulation of uncoupled LHC. Plant Cell Physiol 44:1141–1151

    PubMed  CAS  Google Scholar 

  • Dilworth MF, Gantt E (1981) Phycobilisome-thylakoid topography on photosynthetically active vesicles of Porphyridium cruentum. Plant Physiol 67:608–612

    PubMed  CAS  Google Scholar 

  • Doan J-M, Schoefs B, Ruban AV, Etienne A-L (2003) Changes in the LHCI aggregation state during iron repletion in the unicellular red alga Rhodella violacea. FEBS Lett 533:59–62

    PubMed  CAS  Google Scholar 

  • Dring MJ, Wagner A, Boeskov J, Lüning K (1996) Sensitivity of intertidal and subtidal red algae to UVA and UVB radiation, as monitored by chlorophyll fluorescence measurements: influence of collection depth and season and length of irradiation. Eur J Phycol 31:293–302

    Google Scholar 

  • Enami I, Murayama H, Ohta H, Kamo M, Nakazato K, Shen J-R (1995) Isolation and characterization of a Photosystem II complex from the red alga Cyanidium caldarium: association of cytochrome c-550 and a 12 kDa protein with the complex. Biochim Biophys Acta 1232:208–216

    PubMed  Google Scholar 

  • Enami I, Kikuchi S, Fukuda T, Ohta H, Shen J-R (1998) Binding and functional properties of four extrinsic proteins of photosystem II from a red alga, Cyanidium caldarium, as studied by release-reconstitution experiments. Biochemistry 37:2787–2793

    PubMed  CAS  Google Scholar 

  • Enami I, Yoshihara S, Tohri A, Okumura A, Ohta H, Shen J-R (2000) Cross-reconstitution of various extrinsic proteins and photosystem II complexes from cyanobacteria, red algae and higher plants. Plant Cell Physiol 41:1354–1364

    PubMed  CAS  Google Scholar 

  • Ferreira KN, Iverson TM, Maghlaoui K, Barber J, Iwata S (2004) Architecture of the photosynthetic oxygen-evolving center. Science 303:1831–1838

    PubMed  CAS  Google Scholar 

  • Ficner R, Huber R (1993) Refined crystal structure of phycoerythrin from Porphyridium cruentum at 0.23-nm resolution and localization of the γ subunit. Eur J Biochem 218:103–106

    PubMed  CAS  Google Scholar 

  • Figueroa FL, Conde-Álvarez R, Gómez I (2003a) Relations between electron transport rates determined by pulse amplitude modulated chlorophyll fluorescence and oxygen evolution in macroalgae under different light conditions. Photosynth Res 75:259–275

    PubMed  CAS  Google Scholar 

  • Figueroa FL, Escassi L, Pérez-Rodríguez E, Korbee N, Giles AD, Johnsen G (2003b) Effects of short-term irradiation on photoinhibition and accumulation of mycosporine-like amino acids in sun and shade species of the red algal genus Porphyra. J Photochem Photobiol B 69:21–30

    PubMed  CAS  Google Scholar 

  • Frackowiak D, Ptak A, Gryczynski Z, Gryczynski I, Targowski P, Zelent B (2004) Fluorescence polarization studies of B-phycoerythrin oriented in polymer film. Photochem Photobiol 79:11–20

    PubMed  CAS  Google Scholar 

  • Fujita Y (1999) An evidence indicating that a weak orange light absorbed by phycobilisomes causes inactivation of PSII in cells of the red alga Porphyridium cruentum grown under a weak red light preferentially exciting Chl a. Plant Cell Physiol 40:924–932

    CAS  Google Scholar 

  • Fujita Y (2001) Chromatic variation of the abundance of PSII complexes observed with the red alga Prophyridium cruentum. Plant Cell Physiol 42:1239–1244

    PubMed  CAS  Google Scholar 

  • Gantt E (1981) Phycobilisomes. Ann Rev Plant Physiol 32:327–347

    CAS  Google Scholar 

  • Gantt E, Conti SF (1966a) Phycobiliprotein localization in algae. Brookhaven Syrup Biol 19:393–405

    CAS  Google Scholar 

  • Gantt E, Conti SF (1966b) Granules associated with the chloroplast lamellae of Porphyridium cruentum. J Cell Biol 29:423–434

    PubMed  CAS  Google Scholar 

  • Gantt E, Lipschultz CA (1972) Phycobilisomes of Porphyridium cruentum I. Isolation. J Cell Biol 54:313–324

    PubMed  CAS  Google Scholar 

  • Gantt E, Lipschultz CA (1974) Phycobilisomes of Porphyridium cruentum: pigment analysis. Biochemistry 13:2960–2966

    PubMed  CAS  Google Scholar 

  • Gantt E, Lipschultz CA (1980) Structure and phycobiliprotein composition of phycobilisomes from Griffithsia pacifica (Rhodophyceae). J Phycol 16:394–398

    CAS  Google Scholar 

  • Gantt E, Edwards MR, Conti SF (1968) Ultrastructure of Porphyridium aerugineum, a blue-green colored Rhodophytan. J Phycol 4:65–71

    Google Scholar 

  • Gantt E, Lipschultz CA, Grabowski J, Zimmerman BK (1979) Phycobilisomes from blue-green and red algae: isolation criteria and dissociation characteristics. Plant Physiol 63:615–620

    PubMed  CAS  Google Scholar 

  • Gantt E, Grabowski B, Cunningham FX Jr (2003) Antenna systems of red algae: phycobilisomes with photosystem II and chlorophyll complexes with photosystem I. In: Green BR, Parson WW (eds) Light-harvesting antennas in photosynthesis. Kluwer Academic Publishers, Netherlands, pp 307–322

    Google Scholar 

  • Gao Z-Q, Wang G-C, Tseng C-K (2004) Isolation and characterization of photosystem II of Porphyra yezoensis Ueda. Acta Biochim Biophys Sinica 36:780–785

    CAS  Google Scholar 

  • Gao Z, Meng C, Wang G, Ye N (2008) Isolation and characterization of photosystem II from the filamentous sporophyte of Porphyra yezoensis. Indian J Biochem Biophys 45:244–249

    PubMed  CAS  Google Scholar 

  • Gardian Z, Bumba L, Schrofel A, Herbstova M, Nebesarova J, Vacha F (2007) Organisation of photosystem I and photosystem II in red alga Cyanidium caldarium: encounter of cyanobacterial and higher plant concepts. Biochim Biophys Acta 1767:725–731

    PubMed  CAS  Google Scholar 

  • Glazer AN (1985) Light harvesting by phycobilisomes. Ann Rev Biophys Biophys Chem 14:47–77

    CAS  Google Scholar 

  • Glazer AN, Wedemayer GJ (1995) Cryptomonad biliproteins—an evolutionary perspective. Photosynth Res 46:93–105

    CAS  Google Scholar 

  • Glazer AN, West JA, Chan CF (1982) Phycoerythrins as chemotaxonomic markers in red algae: a survey. Biochem Syst Ecol 10:203–215

    CAS  Google Scholar 

  • Glazer AN, Chan CF, West JA (1996) An unusual phycocyanobilin-containing phycoerythrin of several bluish-colored, acrochaetioid, freshwater red algal species. J Phycol 33:617–624

    Google Scholar 

  • Glöckner G, Rosenthal A, Valentin K (2000) The structure and gene repertoire of an ancient red algal plastid genome. J Mol Evol 51:382–390

    PubMed  Google Scholar 

  • Gómez-Lojero C, Pérez-Gómez B, Shen G, Schluchter WM, Bryant DA (2003) Interaction of ferredoxin:NADP+ oxidoreductase with phycobilisomes and phycobilisome substructures of the cyanobacterium Synechococcus sp.strain. Biochemistry 42:13800–13811

    PubMed  Google Scholar 

  • Grabowski B, Cunningham FX Jr, Gantt E (2001) Chlorophyll and carotenoid binding in a simple red algal light-harvesting complex crosses phylogenetic lines. Proc Natl Acad Sci USA 98:2911–2916

    PubMed  CAS  Google Scholar 

  • Grossman AR, Schaefer MR, Chiang GG, Collier JL (1993) The phycobilisome, a light-harvesting complex responsive to environmental conditions. Microbiol Rev 57:725–749

    PubMed  CAS  Google Scholar 

  • Guglielmi G, Cohen-Bazire G, Bryant DA (1981) The structure of Gloeobacter violaceus and its phycobilisomes. Arch Microbiol 129:181–189

    CAS  Google Scholar 

  • Guskov A, Kern J, Gabdulkhakov A, Broser M, Zouni A, Saenger W (2009) Cyanobacterial photosystem II at 2.9-Ǻ resolution and the role of quinones, lipids, channels and chloride. Nat Struct Mol Biol 16:334–342

    PubMed  CAS  Google Scholar 

  • Häder D-P, Lebert M, Figueroa FL, Jiménez C, Viñegla B, Perez-Rodriguez E (1998) Photoinhibition in Mediterranean macroalgae by solar radiation measured on site by PAM fluorescence. Aquat Bot 61:225–236

    Google Scholar 

  • Häder D-P, Lebert M, Sinha RP, Barbieri ES, Helbling EW (2002) Role of protective and repair mechanisms in the inhibition of photosynthesis in marine macroalgae. Photochem Photobiol Sci 1:809–814

    PubMed  Google Scholar 

  • Häder D-P, Lebert M, Helbling W (2003) Effects of solar radiation on the Patagonian rhodophyte Corallina officinatis (L.). Photosynth Res 78:119–132

    PubMed  Google Scholar 

  • Hagopian JC, Reis M, Kitajima JP, Bhattacharya D, de Oliveira MC (2004) Comparative analysis of the complete plastid genome sequence of the red alga Gracilaria tenuistipitata var. liui provides insights into the evolution of rhodoplasts and their relationship to other plastids. J Mol Evol 59:464–477

    PubMed  CAS  Google Scholar 

  • Hanelt D, Huppertz K, Nultsch W (1992) Photoinhibition of photosynthesis and its recovery in red algae. Bot Acta 105:278–284

    Google Scholar 

  • Ho C-L, Teoh S, Teo S-S, Rahim RA, Phang S-M (2009) Profiling the transcriptome of Gracilaria changii (Rhodophyta) in response to light deprivation. Mar Biotechnol 11:513–519

    PubMed  CAS  Google Scholar 

  • Holzinger A, Lütz C, Karsten U, Wiencke C (2004) The effect of ultraviolet radiation on ultrastructure and photosynthesis in the red macroalgae Palmaria palmata and Odonthalia dentata from Arctic waters. Plant Biol 6:568–577

    PubMed  CAS  Google Scholar 

  • Jahn W, Steinbiss J, Zetsche K (1984) Light intensity adaptation of the phycobiliprotein content of the red alga Porphyridium. Planta 161:536–539

    CAS  Google Scholar 

  • Jiang T, Zhang J-P, Liang D-C (1999) Structure and function of chromophores in R-phycoerythrin at 1.9 Å resolution. Proteins 34:224–231

    PubMed  CAS  Google Scholar 

  • Jiang T, Zhang J-P, Chang W-R, Liang D-C (2001) Crystal structure of R-phycocyanin and possible energy transfer pathways in the phycobilisome. Biophys J 81:1171–1179

    PubMed  CAS  Google Scholar 

  • Jordan P, Fromme P, Witt HT, Klukas O, Saenger W, Krauß N (2001) Three-dimensional structure of cyanobacterial photosystem I at 2.5 Å resolution. Nature 411:909–917

    PubMed  CAS  Google Scholar 

  • Kamiya N, Shen J-R (2003) Crystal structure of oxygen-evolving photosystem II from Thermosynechococcus vulcanus at 3.7-Å resolution. Proc Natl Acad Sci USA 100:98–103

    PubMed  CAS  Google Scholar 

  • Karsten U, Bischof K, Hanelt D, Tüg H, Wiencke C (1999) The effect of ultraviolet radiation on photosynthesis and ultraviolet-absorbing substances in the endemic Arctic macroalga Devaleraea ramentacea (Rhodophyta). Physiol Plantarum 105:58–66

    CAS  Google Scholar 

  • Kawakami T, Sakaguchi K, Takechi K, Takano H, Takio S (2009) Ammonium induced expression of the red algal chloroplast gene Ycf18, a putative homolog of the cyanobacterial NblA gene involved in nitrogen deficiency-induced phycobilisome degradation. Biosci Biotechnol Biochem 73:740–743

    PubMed  CAS  Google Scholar 

  • Klotz AV, Glazer AN (1985) Characterization of the bilin attachment sites in R-phycoerythrin. J Biol Chem 260:4856–4863

    PubMed  CAS  Google Scholar 

  • Koller KP, Wehrmeyer W, Schneider H (1977) Isolation and characterization of disc-shaped phycobilisomes from the red alga Rhodella violacea. Arch Microbiol 112:61–67

    PubMed  CAS  Google Scholar 

  • Koller K-P, Wehrmeyer W, Mörschel E (1978) Biliprotein assemble in the disc-shaped phycobilisomes of Rhodella violacea. On the molecular composition of energy-transfering complexes (tripartite units) forming the periphery of the phycobilisome. Eur J Biochem 91:57–63

    PubMed  CAS  Google Scholar 

  • Kondo K, Geng XX, Katayama M, Ikeuchi M (2005) Distinct roles of CpcG1 and CpcG2 in phycobilisome assembly in the cyanobacterium Synechocystis sp. PCC 6803. Photosynth Res 84:269–273

    PubMed  CAS  Google Scholar 

  • Kondo K, Ochiai Y, Katayama M, Ikeuchi M (2007) The membrane-associated CpcG2-phycobilisome in Synechocystis: a new photosystem I antenna. Plant Physiol 144:1200–1210

    PubMed  CAS  Google Scholar 

  • Kondo K, Mullineaux CW, Ikeuchi M (2009) Distinct roles of CpcG1-phycobilisome and CpcG2-phycobilisome in state transitions in a cyanobacterium Synechocystis sp. PCC 6803. Photosynth Res 99:217–225

    PubMed  CAS  Google Scholar 

  • Korbee N, Figueroa FL, Aguilera J (2005) Effect of light quality on the accumulation of photosynthetic pigments, proteins and mycosporine-like amino acids in the red alga Porphyra leucosticta (Bangiales, Rhodophyta). J Photochem Photobiol B 80:71–78

    PubMed  CAS  Google Scholar 

  • Kursar TA, Alberte RS (1983) Photosynthetic unit organization in a red alga: relationships between light-harvesting pigments and reaction centers. Plant Physiol 72:409–414

    PubMed  CAS  Google Scholar 

  • Kursar TA, van der Meer J, Alberte RS (1983) Light-harvesting system of the red alga Gracilaria tikvahiae: I. Biochemical analyses of pigment mutations. Plant Physiol 73:353–360

    PubMed  CAS  Google Scholar 

  • Lange W, Wilhelm C, Wehrmeyer W, Morschel E (1990) The supramolecular structure of photosystem II-phycobilisome-complexes of Porphyridium cruentum. Bot Acta 103:250–257

    Google Scholar 

  • Levy I, Gantt E (1990) Development of photosynthetic activity in Porphyridium purpureum (Rhodophyta) following nitrogen starvation. J Phycol 26:62–68

    CAS  Google Scholar 

  • Ley AC (1984) Effective absorption cross-sections in Porphyridium cruentum: implications for energy transfer between phycobilisomes and photosystem II reaction centers. Plant Physiol 74:451–454

    PubMed  CAS  Google Scholar 

  • Lichtle C, Garnier F, Bernard C, Zabulon G, Spilar A, Thomas J-C, Etienne A-L (1996) Differential transcription of phycobiliprotein components in Rhodella violacea: light and nitrogen effects on the 33-kilodalton phycoerythrin rod linker polypeptide, phycocyanin, and phycoerythrin transcripts. Plant Physiol 112:1045–1054

    PubMed  CAS  Google Scholar 

  • Liu J-Y, Jiang T, Zhang J-P, Liang D-C (1999) Crystal structure of allophycocyanin from red algae Porphyra yezoensis at 2.2-Å resolution. J Biol Chem 274:16945–16952

    PubMed  CAS  Google Scholar 

  • Liu J, Dong S, Liu X, Ma S (2000) Responses of the macroalga Gracilaria tenuistipitata var. liui (Rhodophyta) to iron stress. J Appl Phycol 12:605–612

    CAS  Google Scholar 

  • Liu L-N, Chen X-L, Zhang X-Y, Zhang Y-Z, Zhou B-C (2005a) One-step chromatography method for efficient separation and purification of R-phycoerythrin from Polysiphonia urceolata. J Biotechnol 116:91–100

    PubMed  CAS  Google Scholar 

  • Liu L-N, Chen X-L, Zhang Y-Z, Zhou B-C (2005b) Characterization, structure and function of linker polypeptides in phycobilisomes of cyanobacteria and red algae: an overview. Biochim Biophys Acta 1708:133–142

    PubMed  CAS  Google Scholar 

  • Liu L-N, Aartsma TJ, Thomas J-C, Lamers GEM, Zhou B-C, Zhang Y-Z (2008a) Watching the native supramolecular architecture of photosynthetic membrane in red algae: topography of phycobilisomes and their crowding, diverse distribution patterns. J Biol Chem 283:34946–34953

    PubMed  CAS  Google Scholar 

  • Liu L-N, Elmalk AT, Aartsma TJ, Thomas J-C, Lamers GEM, Zhou B-C, Zhang Y-Z (2008b) Induced energetic decoupling as a mechanism for phycobilisome-related energy dissipation in red algae: a single molecule study. PLoS ONE 3:e3134

    PubMed  Google Scholar 

  • Liu L-N, Aartsma TJ, Thomas J-C, Zhou B-C, Zhang Y-Z (2009a) FRAP analysis on red alga reveals the fluorescence recovery is ascribed to intrinsic photoprocesses of phycobilisomes than large-scale diffusion. PLoS ONE 4:e5295

    PubMed  Google Scholar 

  • Liu L-N, Su H-N, Yan S-G, Shao S-M, Xie B-B, Chen X-L, Zhang X-Y, Zhou B-C, Zhang Y-Z (2009b) Probing the pH sensitivity of R-phycoerythrin: investigations of active conformational and functional variation. Biochim Biophys Acta 1787:939–946

    PubMed  CAS  Google Scholar 

  • Loll B, Kern J, Saenger W, Zouni A, Biesiadka J (2005) Towards complete cofactor arrangement in the 3.0 Ǻ resolution structure of photosystem II. Nature 438:1040–1044

    PubMed  CAS  Google Scholar 

  • Lüder UH, Knoetzel J, Wiencke C (2001) Two forms of phycobilisomes in the Antarctic red macroalga Palmaria decipiens (Palmariales, Florideophyceae). Physiol Plantarum 112:572–581

    Google Scholar 

  • Ma Y, Xie J, Zhang R, Hua C, Zhao J (2008) Molecular properties of R-phycocyanin subunits from Polysiphonia urceolata in potassium phosphate buffer. Photochem Photobiol Sci 7:263–268

    PubMed  CAS  Google Scholar 

  • MacColl R (1998) Cyanobacterial phycobilisomes. J Struct Biol 124:311–334

    PubMed  CAS  Google Scholar 

  • MacColl R, Eisele LE, Williams EC, Bowser SS (1996) The discovery of a novel R-phycoerythrin from an antarctic red alga. J Biol Chem 271:17157–17160

    PubMed  CAS  Google Scholar 

  • Marquardt J, Rehm AM (1995) Porphyridium purpureum (Rhodophyta) from red and green light: characterization of photosystem I and determination of in situ fluorescence spectra of the photosystems. J Photochem Photobiol B 30:49–56

    CAS  Google Scholar 

  • Marquardt J, Rhiel E (1997) The membrane-intrinsic light-harvesting complex of the red alga Galdieria sulphuraria (formerly Cyanidium caldarium): biochemical and immunochemical characterization. Biochim Biophys Acta 1320:153–164

    CAS  Google Scholar 

  • Marquardt J, Schultze A, Rosenkranz V, Wehrmeyer W (1999) Ultrastructure and photosynthetic apparatus of Rhodella violacea (porphyridiales, rhodophyta) grown under iron-deficient conditions. Phycologia 38:418–427

    Google Scholar 

  • Marquardt J, Wans S, Rhiel E, Randolf A, Krumbein WE (2000) Intron-exon structure and gene copy number of a gene encoding for a membrane-intrinsic light-harvesting polypeptide of the red alga Galdieria sulphuraria. Gene 255:257–265

    PubMed  CAS  Google Scholar 

  • Marquardt J, Lutz B, Wans S, Rhiel E, Krumbein WE (2001) The gene family coding for the light-harvesting polypeptides of Photosystem I of the red alga Galdieria sulphuraria. Photosynth Res 68:121–130

    PubMed  CAS  Google Scholar 

  • Matsuzaki M, Misumi O, Shin-i T, Maruyama S, Takahara M, Miyagishima S-y, Mori T, Nishida K, Yagisawa F, Nishida K, Yoshida Y, Nishimura Y, Nakao S, Kobayashi T, Momoyama Y, Higashiyama T, Minoda A, Sano M, Nomoto H, Oishi K, Hayashi H, Ohta F, Nishizaka S, Haga S, Miura S, Morishita T, Kabeya Y, Terasawa K, Suzuki Y, Ishii Y, Asakawa S, Takano H, Ohta N, Kuroiwa H, Tanaka K, Shimizu N, Sugano S, Sato N, Nozaki H, Ogasawara N, Kohara Y, Kuroiwa T (2004) Genome sequence of the ultrasmall unicellular red alga Cyanidioschyzon merolae 10D. Nature 428:653–657

    PubMed  CAS  Google Scholar 

  • Mercado JM, Sánchez P, Carmona R, Niell FX (2002) Limited acclimation of photosynthesis to blue light in the seaweed Gracilaria tenuistipitata. Physiol Plantarum 114:491–498

    CAS  Google Scholar 

  • Mimuro M, Kikuchi H (2003) Antenna systems and energy transfer in Cyanophyta and Rhodophyta. In: Green BR, Parson WW (eds) Light-harvesting antennas in photosynthesis. Kluwer Academic Publishers, Netherlands, pp 281–306

    Google Scholar 

  • Mörschel E, Koller KP, Wehrmeyer W, Schneider H (1977) Biliprotein assembly in the disc-shaped phycobilisomes of Rhodella violacea, I. Electron microscopy of phycobilisomes in situ and analysis of their architecture after isolation and negtive staining. Cytobiologie 16:118–129

    Google Scholar 

  • Morsy FM, Nakajima M, Yoshida T, Fujiwara T, Sakamoto T, Wada K (2008) Subcellular localization of ferredoxin-NADP+ oxidoreductase in phycobilisome retaining oxygenic photosysnthetic organisms. Photosynth Res 95:73–85

    PubMed  CAS  Google Scholar 

  • Mullineaux CW (1994) Excitation energy transfer from phycobilisomes to photosystem I in a cyanobacterial mutant lacking photosystem II. Biochim Biophys Acta 1184:71–77

    CAS  Google Scholar 

  • Mullineaux CW (2008) Phycobilisome-reaction centre interaction in cyanobacteria. Photosynth Res 95:175–182

    Google Scholar 

  • Mullineaux CW, Tobin MJ, Jones GR (1997) Mobility of photosynthetic complexes in thylakoid membranes. Nature 390:421–424

    CAS  Google Scholar 

  • Mustardy L, Cunningham FX Jr, Gantt E (1992) Photosynthetic membrane topography: Quantitative in situ localization of photosystems I and II. Proc Natl Acad Sci USA 89:10021–10025

    PubMed  CAS  Google Scholar 

  • Neushul M (1970) A freeze-etching study of the red alga Porphyridium. Am J Bot 57:1231–1239

    Google Scholar 

  • Neushul M (1971) Uniformity of thylakoid structure in a red, a brown and two blue-green algae. J Ultrastruct Res 37:532–543

    PubMed  CAS  Google Scholar 

  • Nikaido I, Asamizu E, Nakajima M, Nakamura Y, Saga N, Tabata S (2000) Generation of 10, 154 expressed sequence tags from a leafy gametophyte of a marine red alga, Porphyra yezoensis. DNA Res 7:223–227

    PubMed  Google Scholar 

  • Niu J-F, Wang G-C, Zhou B-C, Lin X-Z, Chen C-S (2007) Purification of R-phycoerythrin from Porphyra haitanensis (Bangiales, Rhodophyta) using expanded-bed absorption. J Phycol 43:1339–1347

    CAS  Google Scholar 

  • Nugent JHA, Purton S, Evans MCW (2003) Oxygenic photosynthesis in algae and cyanobacteria: electron transfer in photosystem I and II. In: Larkum AWD, Douglas S, Raven JA (eds) Photosynthesis in algae. Kluwer Academic Publishers, Netherlands, pp 133–156

    Google Scholar 

  • Ohta H, Suzuki T, Ueno M, Okumura A, Yoshihara S, Shen J-R, Enami I (2003a) Extrinsic proteins of photosystem II; an intermediate member of PsbQ protein family in red algal PS II. Eur J Biochem 270:4156–4163

    PubMed  CAS  Google Scholar 

  • Ohta N, Matsuzaki M, Misumi O, Miyagishima S-Y, Nozaki H, Tanaka K, Shin-I T, Kohara Y, Kuroiwa T (2003b) Complete sequence and analysis of the plastid genome of the unicellular red alga Cyanidioschyzon merolae. DNA Res 10:67–77

    PubMed  CAS  Google Scholar 

  • Pan ZZ, Zhou BC, Tseng CK (1986) Comparative studies on spectral properties of R-phycoerythrin from the red seaweeds from Qingdao. Chin J Oceanol Limnol 4:353–359

    Google Scholar 

  • Pan J, Shi D, Chen J, Peng G, Zeng C, Qiyuan Z (2001) Excitation energy distribution between two photosystems in Porphyra yezoensis and its significance in photosynthesis evolution. Chinese Sci Bull 46:1–4

    Google Scholar 

  • Redecker D, Wehrmeyer W, Reuter W (1993) Core substructure of the hemiellipsoidal phycobilisome from the red alga Porphyridium cruentum. Eur J Cell Biol 62:442–450

    PubMed  CAS  Google Scholar 

  • Redlinger T, Gantt E (1981) Phycobilisome structure of Porphyridium cruentum: polypeptide composition. Plant Physiol 68:1375–1379

    PubMed  CAS  Google Scholar 

  • Reith M, Munholland J (1993) A high-resolution gene map of the chloroplast genome of the red alga Porphyra purpurea. Plant Cell 5:465–475

    PubMed  CAS  Google Scholar 

  • Reith M, Munholland J (1995) Complete nucleotide sequence of the Porphyra purpurea chloroplast genome. Plant Mol Biol Rep 13:333–335

    CAS  Google Scholar 

  • Rennis DS, Ford TW (1992) A survey of antigenic differences between phycoerythrins of various red algal (Rhodophyta) species. Phycologia 31:192–204

    Google Scholar 

  • Reuter W, Wiegand G, Huber R, Than ME (1999) Structural analysis at 2.2 Ǻ of orthorhombic crystals presents the asymmetry of the allophycocyanin-linker complex, AP L 7.8C , from phycobilisomes of Mastigocladus laminosus. Proc Natl Acad Sci USA 96:1363–1368

    PubMed  CAS  Google Scholar 

  • Ritter S, Hiller RG, Wrench PM, Welte W, Diederichs K (1999) Crystal structure of a phycourobilin-containing phycoerythrin at 1.90-Ǻ resolution. J Struct Biol 126:86–97

    PubMed  CAS  Google Scholar 

  • Ritz M, Lichtlé C, Spilar A, Joder A, Thomas J-C, Etienne A-L (1998) Characterization of phycocyanin-deficient phycobilisomes from a pigment mutant of Porphyridium sp. (Rhodophyta). J Phycol 34:835–843

    CAS  Google Scholar 

  • Ritz M, Thomas J-C, Spilar A, Etienne A-L (2000) Kinetics of photoacclimation in response to a shift to high light of the red alga Rhodella violacea adapted to low irradiance. Plant Physiol 123:1415–1425

    PubMed  CAS  Google Scholar 

  • Román RB, Alvárez-Pez JM, Fernández FGA, Grima EM (2002) Recovery of pure B-phycoerythrin from the microalga Porphyridium cruentum. J Biotechnol 93:73–85

    Google Scholar 

  • Rowan KS (1989) Photosynthetic pigments of algae. Cambridge University Press, Cambridge, pp 166–211

    Google Scholar 

  • Sagert S, Schubert H (1995) Acclimation of the photosynthetic apparatus of Palmaria palmata (Rhodophyta) to light qualities that preferentially excite photosystem I or photosystem II. J Phycol 31:547–554

    CAS  Google Scholar 

  • Samsonoff WA, MacColl R (2001) Biliproteins and phycobilisomes from cyanobacteria and red algae at the extremes of habitat. Arch Microbiol 176:400–405

    PubMed  CAS  Google Scholar 

  • Scheer H, Zhao K-H (2008) Biliprotein maturation: the chromophore attachment. Mol Microbiol 68:263–276

    PubMed  CAS  Google Scholar 

  • Scheuring S, Sturgis JN (2009) Atomic force microscopy of the bacterial photosynthetic apparatus: plain pictures of an elaborate machinery. Photosynth Res 102:197–211

    CAS  Google Scholar 

  • Sheath RG, Hellebust JA, Sawa T (1977) Changes in plastid structure, pigmentation and photosynthesis of the conchocelis stage of Porphyra leucosticta (Rhodophyta, Bangiophyceae) in response to low light and darkness. Phycologia 16:265–276

    Google Scholar 

  • Shen J-R, Inoue Y (1993) Binding and functional properties of two new extrinsic components, cytochrome c-550 and a 12-kDa protein, in cyanobacterial photosystem II. Biochemistry 32:1825–1832

    PubMed  CAS  Google Scholar 

  • Shen G, Boussiba S, Vermaas WFJ (1993) Synechocystis sp PCC 6803 strains lacking photosystem I and phycobilisome function. Plant Cell 5:1853–1863

    PubMed  CAS  Google Scholar 

  • Sidler W (1994) Phycobilisomes and phycobiliprotein structures. In: Bryant DA (ed) The molecular biology of Cyanobacteria. Kluwer Academic Publishers, Netherlands, pp 139–216

    Google Scholar 

  • Stadnichuk IN, Idintsova TI, Strongin AY (1984) Molecular organization and pigment composition of R-phycoerythrin from the red alga Callithamnion rubosum. Mol Biol (Moscow) 18:343–349

    CAS  Google Scholar 

  • Stadnichuk IN, Khokhlachev AV, Tikhonova YV (1993) Polypeptide γ-subunits of R-phycoerythrin. J Photochem Photobiol B 18:169–175

    CAS  Google Scholar 

  • Stadnichuk IN, Karapetyan NV, Kislov LD, Semenenko VE, Veryasov MB (1997) Two γ-polypeptides of B-phycoerythrin from Porphyridium cruentum. J Photochem Photobiol B 39:19–23

    CAS  Google Scholar 

  • Staehelin LA, Giddings TH, Badami P, Krzymowski WW (1978) A comparison of the supramolecular architecture of photosynthetic membranes of blue-green, red, and green algae and of higher plants. In: Deamer D (ed) Light transducing membranes. Academic Press, New York, pp 335–355

    Google Scholar 

  • Stec B, Troxler RF, Teeter MM (1999) Crystal structure of C-phycocyanin from Cyanidium caldarium provides a new perspective on phycobilisome assembly. Biophys J 76:2912–2921

    PubMed  CAS  Google Scholar 

  • Sturgis JN, Tucker JD, Olsen JD, Hunter CN, Niederman RA (2009) Atomic force microscopy studies of native photosynthetic membranes. Biochemistry 48:3679–3698

    PubMed  CAS  Google Scholar 

  • Sun L, Wang S, Gong X, Zhao M, Fu X, Wang L (2009) Isolation, purification and characteristics of R-phycoerythrin from a marine macroalga Heterosiphonia japonica. Protein Expres Purif 64:146–154

    CAS  Google Scholar 

  • Takahashi T, Inoue-Kashino N, Ozawa S-i, Takahashi Y, Kashino Y, Satoh K (2009) Photosystem II complex in vivo is a monomer. J Biol Chem 284:15598–15606

    PubMed  CAS  Google Scholar 

  • Talarico L (1990) R-Phycoerythrin from Audoniella saviana (Nemaliales, Rhodophyta)—ultrastructural and biochemical analysis of aggregates and subunits. Phycologia 29:292–302

    Google Scholar 

  • Talarico L (1996) Phycobiliproteins and phycobilisomes in red algae: adaptive responses to light. Sci Mar 60((Supl. 1)):205–222

    CAS  Google Scholar 

  • Talarico L, Cortese A (1993) Response of Audouinella saviana (Meneghini) Woelkerling (Nemaliales, Rhodophyta) cultures to monochromatic light. Hydrobiologia 260–261:477–484

    Google Scholar 

  • Talarico L, Maranzana G (2000) Light and adaptive responses in red macroalgae: an overview. J Photochem Photobiol B 56:1–11

    PubMed  CAS  Google Scholar 

  • Tan S, Wolfe GR, Cunningham FX Jr, Gantt E (1995) Decrease of polypeptides in the PS I antenna complex with increasing growth irradiance in the red alga Porphyridium cruentum. Photosynth Res 45:1–10

    CAS  Google Scholar 

  • Tan S, Cunningham FX Jr, Gantt E (1997a) LhcaR1 of the red alga Porphyridium cruentum encodes a polypeptide of the LHCI complex with seven potential chlorophyll a-binding residues that are conserved in most LHCs. Plant Mol Biol 33:157–167

    PubMed  CAS  Google Scholar 

  • Tan S, Ducret A, Aebersold R, Gantt E (1997b) Red algal LHC I genes have similarities with both Chl a/b- and a/c-binding proteins: a 21 kDa polypeptide encoded by LhcaR2 is one of the six LHC I polypeptides. Photosynth Res 53:129–140

    CAS  Google Scholar 

  • Toole CM, Allnutt FCT (2003) Red, cryptomonad and glaucocystophyte algal phycobiliproteins. In: Larkum AWD, Douglas S, Raven JA (eds) Photosynthesis in algae. Kluwer Academic Publishers, Netherlands, pp 305–334

    Google Scholar 

  • Tsekos I, Reiss H-D (1988) Freeze-fractured thylakoids of some marine red algae. Phyton 28:201–214

    Google Scholar 

  • Tsekos I, Reiss H-D, Orfanidis S, Orologas N (1996) Ultrastructure and supramolecular organization of photosynthetic membranes of some marine red algae. New Phytol 133:543–551

    Google Scholar 

  • Tsekos I, Niell FX, Aguilera J, Figueroa FL, Delivopoulos SG (2002) Ultrastructure of the vegetative gametophytic cells of Porphyra leucosticta (Rhodophyta) grown in red, blue and green light. Phycol Res 50:251–264

    Google Scholar 

  • Tsekos I, Reiss H-D, Delivopoulos SG (2004) The supramolecular organization of photosynthetic membranes in the red alga Thorea ramosissisma: spatial relationship between putative photosystem II core particles (EF-particles) and phycobilisomes. Phycologia 43:543–551

    Google Scholar 

  • van Thor JJ, Gruters OW, Matthijs HC, Hellingwerf KJ (1999) Localization and function of ferredoxin:NADP(+) reductase bound to the phycobilisomes of Synechocystis. EMBO J 18:4128–4136

    PubMed  Google Scholar 

  • Vanselow C, Weber APM, Krause K, Fromme P (2009) Genetic analysis of the Photosystem I subunits from the red alga, Galdieria sulphuraria. Biochim Biophys Acta 1787:46–59

    PubMed  CAS  Google Scholar 

  • Villafañe VE, Gao K, Helbling EW (2005) Short- and long-term effects of solar ultraviolet radiation on the red algae Porphyridium cruentum (S. F. Gray) Nägeli. Photochem Photobiol Sci 4:376–382

    PubMed  Google Scholar 

  • Waaland JR, Waaland SD, Bates G (1974) Chloroplast structure and pigment composition in the red algae Griffithsia pacifica: regulation by light intensity. J Phycol 10:193–199

    Google Scholar 

  • Wanner G, Köst H-P (1980) Investigations on the arrangement and fine structure of Porphyridium cruentum phycobilisomes. Protoplasma 102:97–109

    Google Scholar 

  • Watanabe M, Iwai M, Narikawa R, Ikeuchi M (2009) Is the photosystem II complex a monomer or a dimer? Plant Cell Physiol 50:1674–1680

    PubMed  CAS  Google Scholar 

  • Weber APM, Oesterhelt C, Gross W, Bräutigam A, Imboden LA, Krassovskaya I, Linka N, Truchina J, Schneidereit J, Voll H, Voll LM, Zimmermann M, Jamai A, Riekhof WR, Yu B, Garavito RM, Benning C (2004) EST-analysis of the thermo-acidophilic red microalga Galdieria sulphuraria reveals potential for lipid A biosynthesis and unveils the pathway of carbon export from rhodoplasts. Plant Mol Biol 55:17–32

    PubMed  CAS  Google Scholar 

  • Wehrmeyer W, Mörschel E, Vogel K (1993) Core substructure in phycobilisomes of red algae. II. The central part of the tricylindrical core–APCM–a constituent of hemidiscoidal phycobilisomes of Rhodella violacea. Eur J Cell Biol 60:203–209

    PubMed  CAS  Google Scholar 

  • Wolfe GR, Cunningham FX, Grabowskia B, Gantt E (1994a) Isolation and characterization of Photosystems I and II from the red alga Porphyridium cruentum. Biochim Biophys Acta 1787:121–128

    Google Scholar 

  • Wolfe GR, Cunningham FX Jr, Durnfordt D, Green BR, Gantt E (1994b) Evidence for a common origin of chloroplasts with light-harvesting complexes of different pigmentation. Nature 367:566–568

    CAS  Google Scholar 

  • Yu M-H, Glazer AN, Spencer KG, West JA (1981) Phycoerythrins of the red alga Caiithamnion: variation in phycoerythrobilin and phycourobilin content. Plant Physiol 68:482–488

    PubMed  CAS  Google Scholar 

  • Zilinskas BA, Greenwald LS (1986) Phycobilisome structure and function. Photosynth Res 10:7–35

    CAS  Google Scholar 

Download references

Acknowledgments

The work was supported by the National Natural Science Foundation of China (40806056), Hi-Tech Research and Development Program of China (2008AA09Z404), Key International S&T Cooperation Project of China (2008DFA30440).

Author information

Authors and Affiliations

  1. The State Key Lab of Microbial Technology, Marine Biotechnology Research Center, Shandong University, Jinan, 250100, People’s Republic of China

    Hai-Nan Su, Bin-Bin Xie, Xi-Ying Zhang, Bai-Cheng Zhou & Yu-Zhong Zhang

Authors
  1. Hai-Nan Su
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Bin-Bin Xie
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Xi-Ying Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Bai-Cheng Zhou
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Yu-Zhong Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Yu-Zhong Zhang.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Su, HN., Xie, BB., Zhang, XY. et al. The supramolecular architecture, function, and regulation of thylakoid membranes in red algae: an overview. Photosynth Res 106, 73–87 (2010). https://doi.org/10.1007/s11120-010-9560-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11120-010-9560-x

Keywords

Search

Navigation