Skip to main content

Light Harvesting by Long-Wavelength Chlorophyll Forms (Red Forms) in Algae: Focus on their Presence, Distribution and Function

  • Chapter
  • First Online:
Photosynthesis in Algae: Biochemical and Physiological Mechanisms

Abstract

The efficiency by which oxygenic photosynthetic organisms, and particularly microalgae, utilise near infrared radiation for sustaining metabolic processes has attracted attention since the pioneering studies of Emerson and coworkers. In the vast majority of photosynthetic organisms, which use Chlorophyll (Chl) a as their main light harvesting as well as photochemically active pigment, the capacity of absorbing incident photons at wavelengths longer than 700 nm is associated with the presence of specific Chl a spectral forms, known as “red forms”. These have been considered to be almost exclusively, and rather ubiquitously, associated to either the core or the external light harvesting apparatus of Photosystem I (PSI). Therefore a large body of information has been gathered, concerning red forms associated with either the core antenna of cyanobacteria or the external light harvesting complexes of green algae as well as those of higher plants which share a common structural architecture. On the other hand, recent ecophysiological in field measurements, together with studies performed in the laboratory on model red clade organisms, challenged this general consensus. In field measurements put in evidence that the presence of PSI red forms, particularly in oceanic waters, is probably less diffused than generally assumed on the basis of model organisms analysis. Moreover, the study of red clade algae demonstrated the presence of red spectral forms associated also to Photosystem II (PSII), particularly under conditions of culture self-shading or growth under far-red illumination. Therefore, in this review chapter the nature and photophysical/photophysiological role of red forms associated to both PSI and PSII will be surveyed and discussed. Moreover a general discussion of the impact of antenna forms absorbing at lower energies than the respective reaction centres, therefore being in competition for excited state localisation with photochemical processes and productive photon energy utilisation, will be discussed in a simplified, although generalised, framework.

*Author for correspondence, e-mail: stefano.santabarbara@cnr.it

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

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 189.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 249.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 249.99
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

References

  • Acuña AM, Lemaire C, van Grondelle R, Robert B, van Stokkum IHM (2018) Energy transfer and trapping in Synechococcus WH7803. Photosynth Res 135:115–124

    Article  PubMed  CAS  Google Scholar 

  • Alboresi A, Caffarri S, Nogue F, Bassi R, Morosinotto T (2008) In Silico and biochemical analysis of Physcomitrella patens photosynthetic antenna: identification of subunits which evolved upon land adaptation. PLoS One 3:e2033

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Alboresi A, Gerotto C, Cazzaniga S, Bassi R, Morosinotto T (2011) A red-shifted antenna protein associated with photosystem II in Physcomitrella patens. J Biol Chem 286:28978–28987

    Article  CAS  PubMed  PubMed Central  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

    Article  CAS  PubMed  Google Scholar 

  • Anderson JM, Boardman NK (1965) Fractionation of photochemical systems of photosynthesis. I. Chlorophyll contents and photochemical activities of particles isolated from spinach chloroplasts. Biochim Biophys Acta 112:403–421

    Article  Google Scholar 

  • Averina S, Velichko N, Senatskaya E, Pinevich A (2018) Far-red light photoadaptations in aquatic cyanobacteria. Hydrobiologia 813:1–17

    Article  CAS  Google Scholar 

  • Bald D, Kruip J, Rögner M (1996) Supramolecular architecture of cyanobacterial thylakoid membranes: how is the phycobilisome connected with the photosystems? Photosynth Res 49:103–118

    Article  CAS  PubMed  Google Scholar 

  • Barter LCM, Durrant JR, Klug DR (2003) A quantitative structure-function relationship for the Photosystern II reaction center: supermolecular behavior in natural photosynthesis. Proc Natl Acad Sci U S A 100:946–951

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bassi R, Soen SY, Frank G, Zuber H, Rochaix JD (1992) Characterization of chlorophyll a/b proteins of photosystem I from Chlamydomonas reinhardtii. J Biol Chem 267:25714–25721

    Article  CAS  PubMed  Google Scholar 

  • Behrendt L, Larkum AWD, Norman A, Qvortrup K, Chen M, Ralph P, Sorensen SJ, Trampe E, Kuhl M (2011) Endolithic chlorophyll d-containing phototrophs. ISME J 5:1072–1076

    Article  CAS  PubMed  Google Scholar 

  • Belgio E, Santabarbara S, Bína D, Trsková E, Herbstová M, Kaňa R, Zucchelli G, Prášil O (2017) High photochemical trapping efficiency in photosystem I from the red clade algae Chromera velia and Phaeodactylum tricornutum. Biochim Biophys Acta 1858:56–66

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Bina D, Gardian Z, Herbstova M, Kotabova E, Konik P, Litvin R, Prášil O, Tichy J, Vacha F (2014) Novel type of red-shifted chlorophyll a antenna complex from Chromera velia: II. Biochemistry and spectroscopy. Biochim Biophys Acta 1837:802–810

    Article  CAS  PubMed  Google Scholar 

  • Boardman NK, Anderson JM (1964) Isolation from spinach chloroplasts of particles containing different proportions of chlorophyll a and chlorophyll b and their possible role in the light reaction of photosynthesis. Nature 203:166–167

    Article  CAS  Google Scholar 

  • Brettel K (1997) Electron transfer and arrangement of the redox cofactors in photosystem I. Biochim Biophys Acta 1318:322–373

    Article  CAS  Google Scholar 

  • Broess K, Trinkunas G, van Hoek A, Croce R, van Amerongen H (2008) Determination of the excitation migration time in photosystem II – consequences for the membrane organization and charge separation parameters. Biochim Biophys Acta 1777:404–409

    Article  CAS  PubMed  Google Scholar 

  • Brown JS (1967) Fluorometric evidence for the participation of chlorophyll a-695 in system 2 of photosynthesis. Biochim Biophys Acta 143:391–398

    Article  CAS  PubMed  Google Scholar 

  • Burki F, Okamoto N, Pombert J-F, Keeling PJ (2012) The evolutionary history of haptophytes and cryptophytes: phylogenomic evidence for separate origins. Proc R Soc B Biol Sci 279(2012):2246–2254

    Article  Google Scholar 

  • Butler WL (1960) A far red absorbing form of chlorophyll. Biochem Biophys Res Commun 3:685–688

    Article  CAS  PubMed  Google Scholar 

  • Butler WL (1961) A far-red absorbing form of chlorophyll, in vivo. Arch Biochem Biophys 93:413–422

    Article  CAS  PubMed  Google Scholar 

  • Butler WL (1978) Energy distribution in the photochemical apparatus of photosynthesis. Annu Rev Plant Physiol 29:345–378

    Article  CAS  Google Scholar 

  • Byrdin M, Rimke I, Schlodder E, Stehlik D, Roelofs TA (2000) Decay kinetics and quantum yields of fluorescence in photosystem I from Synechococcus elongatus with P700 in the reduced and oxidized state: are the kinetics of excited state decay trap-limited or transfer-limited? Biophys J 79:992–100

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Byrdin M, Jordan P, Krauss N, Fromme P, Stehlik D, Schlodder E (2002) Light harvesting in photosystem I: modeling based on the 2.5-angstrom structure of photosystem I from Synechococcus elongatus. Biophys J 83:433–457

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Caffarri S, Broess K, Croce R, van Amerongen H (2011) Excitation energy transfer and trapping in higher plant photosystem II complexes with different antenna sizes. Biophys J 100:2094–2103

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Caffarri S, Tibiletti T, Jennings RC, Santabarbara S (2014) A comparison between plant photosystem I and photosystem II architecture and functioning. Curr Protein Pept Sci 15:296–331

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Castelletti S, Morosinotto T, Robert B, Caffarri S, Bassi R, Croce R (2003) Recombinant Lhca2 and Lhca3 subunits of the photosystem I antenna system. Biochemistry 42:4226–4234

    Article  CAS  PubMed  Google Scholar 

  • Chen M, Schliep M, Willows RD, Cai ZL, Neilan BA, Scheer H (2010) A red-shifted chlorophyll. Science 329:1318–1319

    Article  CAS  PubMed  Google Scholar 

  • Cho F, Govindjee (1970a) Fluorescence spectra of Chlorella in the 295-77°K range. Biochim Biophys Acta 205:371–378

    Article  CAS  PubMed  Google Scholar 

  • Cho F, Govindjee (1970b) Low-temperature (4-77°K) spectroscopy of Chlorella; temperature dependence of energy transfer efficiency. Biochim Biophys Acta 216:139–150

    Article  CAS  PubMed  Google Scholar 

  • Chua NH, Matlin K, Bennoun P (1975) A chlorophyll-protein complex lacking in photosystem I mutants of Chlamydomonas reinhardtii. J Cell Biol 67:361–377

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cometta A, Zucchelli G, Karapetyan NV, Engelmann E, Garlaschi FM, Jennings RC (2000) Thermal behavior of long wavelength absorption transitions in Spirulina platensis photosystem I trimers. Biophys J 79:3235–3243

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Croce R, van Amerongen H (2013) Light-harvesting in photosystem I. Photosynth Res 116:153–166

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Croce R, Zucchelli G, Garlaschi FM, Bassi R, Jennings RC (1996) Excited state equilibration in the photosystem I-light-harvesting I complex: P700 is almost isoenergetic with its antenna. Biochemistry 35:8572–8579

    Article  CAS  PubMed  Google Scholar 

  • Croce R, Zucchelli G, Garlaschi FM, Jennings RC (1998) A thermal broadening study of the antenna chlorophylls in PSI-200, LHCI, and PSI core. Biochemistry 37:17355–17360

    Article  CAS  PubMed  Google Scholar 

  • Croce R, Dorra D, Holzwarth AR, Jennings RC (2000) Fluorescence decay and spectral evolution in intact photosystem I of higher plants. Biochemistry 39:6341–6348

    Article  CAS  PubMed  Google Scholar 

  • Croce R, Morosinotto T, Castelletti S, Breton J, Bassi R (2002) The Lhca antenna complexes of higher plants photosystem I. Biochim Biophys Acta 1556:29–40

    Article  CAS  PubMed  Google Scholar 

  • Croce R, Morosinotto T, Ihalainen JA, Chojnicka A, Breton J, Dekker JP, van Grondelle R, Bassi R (2004) Origin of the 701-nm fluorescence emission of the Lhca2 subunit of higher plant photosystem I. J Biol Chem 279:48543–48549

    Article  CAS  PubMed  Google Scholar 

  • Croce R, Chojnicka A, Morosinotto T, Ihalainen JA, van Mourik F, Dekker JP, Bassi R, van Grondelle R (2007) The low-energy forms of photosystem I light-harvesting complexes: spectroscopic properties and pigment-pigment interaction characteristics. Biophys J 93:2418–2428

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Damjanovic A, Vaswani HM, Fromme P, Fleming GR (2002) Chlorophyll excitations in photosystem I of Synechococcus elongatus. J Phys Chem B 106:10251–10262

    Article  CAS  Google Scholar 

  • Döring G, Stiel HH, Witt HT (1967) A second chlorophyll reaction in the electron chain of photosynthesis – registration by the repetitive excitation technique. Z Naturforsch 22B:639–644

    Article  Google Scholar 

  • Döring G, Bailey JR, Weikara J, Witt HT (1968) Some new results in photosynthesis, the action of two chlorophyll a molecules in light reaction I of photosynthesis. Naturwissenschaften 5:219–224

    Article  Google Scholar 

  • Drop B, Yadav SKN, Boekema EJ, Croce R (2014) Consequences of state transitions on the structural and functional organization of photosystem I in the green alga Chlamydomonas reinhardtii. Plant J 78:181–191

    Article  CAS  PubMed  Google Scholar 

  • Duysens LNM (1978) Transfer and trapping of excitation energy in photosystem II. CIBA Found Symp 323–340

    Google Scholar 

  • Duysens LNM, Amesez J, Kamp BM (1961) Two photochemical system in photosynthesis. Nature 190:510–511

    Article  CAS  PubMed  Google Scholar 

  • Emerson R, Arnold W (1932) Separation of the reactions in photosynthesis by means of intermittent light. J Gen Physiol 15:391–420

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Emerson R, Lewis CM (1943) The dependence of the quantum yield of chlorella photosynthesis on wavelength of light. Am J Bot 30:165–178

    Article  CAS  Google Scholar 

  • Emerson R, Rabinowitch E (1960) Red drop and the role of auxiliary pigments in photosynthesis. Plant Physiol 35:477–485

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Emerson R, Chalmers RV, Cederstrand C (1957) Some factors influencing the long-wave limit of photosynthesis. Proc Natl Acad Sci U S A 43:133–143

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Engelmann ECM, Zucchelli G, Garlaschi FM, Casazza AP, Jennings RC (2005) The effect of outer antenna complexes on the photochemical trapping rate in barley thylakoid photosystem II. Biochim Biophys Acta 1706:276–286

    Article  CAS  PubMed  Google Scholar 

  • Engelmann ECM, Zucchelli G, Casazza AP, Brogioli D, Garlaschi FM, Jennings RC (2006) Influence of the photosystem I-light harvesting complex I antenna domains on fluorescence decay. Biochemistry 45:6947–6955

    Article  CAS  PubMed  Google Scholar 

  • French CS (1967) Changes with age in absorption spectrum of chlorophyll a in a diatom. Archiv Fur Mikrobiologie 59:93–103

    Article  CAS  PubMed  Google Scholar 

  • French CS (1971) The distribution and action in photosynthesis of several forms of chlorophyll. Proc Natl Acad Sci U S A 68:2893–2897

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fromme P, Jordan P, Krauss N (2001) Structure of photosystem I. Biochim Biophys Acta 1507:5–31

    Article  CAS  PubMed  Google Scholar 

  • Fujita Y, Ohki K (2004) On the 710 nm fluorescence emitted by the diatom Phaeodactylum tricornutum at room temperature. Plant Cell Physiol 45:392–397

    Article  CAS  PubMed  Google Scholar 

  • Galka P, Santabarbara S, Khuong TT, Degand H, Morsomme P, Jennings RC, Boekema EJ, Caffarri S (2012) Functional analyses of the plant photosystem I-light-harvesting complex II supercomplex reveal that light-harvesting complex II loosely bound to photosystem II is a very efficient antenna for photosystem I in state II. Plant Cell 24:2963–2978

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gan F, Bryant DA (2015) Adaptive and acclimative responses of cyanobacteria to far-red light. Environ Microbiol 17:3450–3465

    Article  CAS  PubMed  Google Scholar 

  • Gan F, Zhang S, Rockwell NC, Martin SS, Lagarias JC, Bryant DA (2014) Extensive remodeling of a cyanobacterial photosynthetic apparatus in far-red light. Science 345:1312–1317

    Article  CAS  PubMed  Google Scholar 

  • Germano M, Yakushevska AE, Keegstra W, van Gorkom HJ, Dekker JP, Boekema EJ (2002) Supramolecular organization of photosystem I and light-harvesting complex I in Chlamydomonas reinhardtii. FEBS Lett 525:121–125

    Article  CAS  PubMed  Google Scholar 

  • Gibasiewicz K, Ramesh VM, Melkozernov AN, Lin S, Woodbury NW, Blankenship RE, Webber AN (2001) Excitation dynamics in the core antenna of PSI from Chlamydomonas reinhardtii CC2696 at room temperature. J Phys Chem B 105:11498–11506

    Article  CAS  Google Scholar 

  • Gibasiewicz K, Szrajner A, Ihalainen JA, Germano M, Dekker JP, van Grondelle R (2005) Characterization of low-energy chlorophylls in the PSI-LHCI supercomplex from Chlamydomonas reinhardtii. A site-selective fluorescence study. J Phys Chem B 109:21180–21186

    Article  CAS  PubMed  Google Scholar 

  • Giera W, Ramesh VM, Webber AN, van Stokkum IHM, van Grondelle R, Gibasiewicz K (2010) Effect of the P700 pre-oxidation and point mutations near A0 on the reversibility of the primary charge separation in photosystem I from Chlamydomonas reinhardtii. Biochim Biophys Acta 1797:106–112

    Article  CAS  PubMed  Google Scholar 

  • Giera W, Szewczyk S, McConnell MD, Snellenburg J, Redding KE, van Grondelle R, Gibasiewicz K (2014) Excitation dynamics in photosystem I from Chlamydomonas reinhardtii. Comparative studies of isolated complexes and whole cells. Biochim Biophys Acta 1837:1756–1768

    Article  CAS  PubMed  Google Scholar 

  • Girard J, Chua NH, Bennoun P, Schmidt G, Delosme M (1980) Studies on mutants deficient in the photosystem I reaction centers in Chlamydomonas reinhardtii. Curr Genet 2:215–221

    Article  CAS  PubMed  Google Scholar 

  • Gobets B, van Grondelle R (2001) Energy transfer and trapping in photosystem I. Biochim Biophys Acta 1057:80–99

    Article  Google Scholar 

  • Gobets B, van Amerongen H, Monshouwer R, Kruip J, Rogner M, van Grondelle R, Dekker JP (1994) Polarised site-selected fluorescence of isolated photosystem I. Biochim Biophys Acta 1188:75–85

    Article  CAS  Google Scholar 

  • Gobets B, van Stokkum IHM, Rogner M, Kruip J, Schlodder E, Karapetyan NV, Dekker JP, van Grondelle R (2001) Time-resolved fluorescence emission measurements of photosystem I particles of various cyanobacteria: a unified compartmental model. Biophys J 81:407–424

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gobets B, Valkunas L, van Grondelle R (2003) Bridging the gap between structural and lattice models: a parameterization of energy transfer and trapping in photosystem I. Biophys J 85:3872–3882

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Govindjee, Rabinowitch E (1960) Two forms of chlorophyll a in vivo with distinct photochemical functions. Science 132:355–356

    Article  CAS  PubMed  Google Scholar 

  • Greenbaum NL, Mauzerall D (1991) Effect of irradiance level on distribution of chlorophylls between PS II and PS I as determined from optical cross-sections. Biochim Biophys Acta 1057:195–207

    Article  CAS  Google Scholar 

  • Halldal P (1968) Photosynthetic capacities and photosynthetic action spectra of endozoic algae of the massive coral favia. Biol Bull 134(3):411–424

    Google Scholar 

  • Hayes JM, Matsuzaki S, Rätsep M, Small GJ (2000) Red chlorophyll a antenna states of photosystem I of the cyanobacterium Synechocystis sp. PCC 6803. J Phys Chem B 104:5625–5633

    Article  CAS  Google Scholar 

  • Herbstova M, Bina D, Konik P, Gardian Z, Vacha F, Litvin R (2015) Molecular basis of chromatic adaptation in pennate diatom Phaeodactylum tricornutum. Biochim Biophys Acta 1847:534–543

    Article  CAS  PubMed  Google Scholar 

  • Herbstova M, Bina D, Kana R, Vacha F, Litvin R (2017) Red-light phenotype in a marine diatom involves a specialized oligomeric red-shifted antenna and altered cell morphology. Sci Rep 7:10

    Article  CAS  Google Scholar 

  • Hill R, Bendall F (1960) Function of the two cytochrome components in chloroplasts: a working hypothesis. Nature 186:136

    Article  CAS  Google Scholar 

  • Hill R, Larkum AWD, Prášil O, Kramer DM, Szabo M, Kumar V, Ralph PJ (2012) Light-induced dissociation of antenna complexes in the symbionts of scleractinian corals correlates with sensitivity to coral bleaching. Coral Reefs 31:963–975

    Article  Google Scholar 

  • Ho MY, Soulier NT, Canniffe DP, Shen G, Bryant DA (2017) Light regulation of pigment and photosystem biosynthesis in cyanobacteria. Curr Opin Plant Biol 37:24–33

    Article  CAS  PubMed  Google Scholar 

  • Hodges M, Moya I (1986) Time-resolved chlorophyll fluorescence studies of photosynthetic membranes: resolution and characterization of four kinetic components. Biochim Biophys Acta 849:193–202

    Article  CAS  Google Scholar 

  • Holzwarth AR, Wendler J, Haehnel W (1985) Time-resolved picosecond fluorescence spectra of the antenna chlorophylls in Chlorella vulgaris. Resolution of photosystem I fluorescence. Biochim Biophys Acta 807:155–167

    Article  CAS  Google Scholar 

  • Holzwarth AR, Müller MG, Niklas J, Lubitz W (2005) Charge recombination fluorescence in photosystem I reaction centers from Chlamydomonas reinhardtii. J Phys Chem B 109:5903–5911

    Article  CAS  PubMed  Google Scholar 

  • Holzwarth AR, Muller MG, Reus M, Nowaczyk M, Sander J, Rogner M (2006) Kinetics and mechanism of electron transfer in intact photosystem II and in the isolated reaction center: Pheophytin is the primary electron acceptor. Proc Natl Acad Sci U S A 103:6895–6900

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hu Q, Miyashita H, Iwasaki I, Kurano N, Miyachi S, Iwaki M, Itoh S (1998) A photosystem I reaction center driven by chlorophyll d in oxygenic photosynthesis. Proc Natl Acad Sci U S A 95:13319–13323

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ihalainen JA, van Stokkum IH, Gibasiewicz K, Germano M, van Grondelle R, Dekker JP (2005a) Kinetics of excitation trapping in intact photosystem I of Chlamydomonas reinhardtii and Arabidopsis thaliana. Biochim Biophys Acta 1706:267–275

    Article  CAS  PubMed  Google Scholar 

  • Ihalainen JA, Klimmek F, Ganeteg U, van Stokkum IH, van Grondelle R, Jansson S, Dekker JP (2005b) Excitation energy trapping in photosystem I complexes depleted in Lhca1 and Lhca4. FEBS Lett 579:4787–4791

    Article  CAS  PubMed  Google Scholar 

  • Itoh S, Mino H, Itoh K, Shigenaga T, Uzumaki T, Iwaki M (2007) Function of chlorophyll d in reaction centers of photosystems I and II of the oxygenic photosynthesis of Acaryochloris marina. Biochemistry 46:12473–12481

    Article  CAS  PubMed  Google Scholar 

  • Jankowiak R, Hayes JM, Small GJ (1993) Spectral hole burning spectroscopy in amorphous molecular solids and proteins. Chem Rev 93:1471–1502

    Article  CAS  Google Scholar 

  • Jennings RC, Zucchelli G, Croce R, Garlaschi FM (2003) The photochemical trapping rate from red spectral states in PSI-LHCI is determined by thermal activation of energy transfer to bulk chlorophylls. Biochim Biophys Acta 1557:91–98

    Article  CAS  PubMed  Google Scholar 

  • Jennings RC, Zucchelli G, Engelmann ECM, Garlaschi FM (2004) The long-wavelength chlorophyll states of plant LHCI at room temperature: a comparison with PSI-LHCI. Biophys J 87:488–497

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jennings RC, Zucchelli G, Santabarbara S (2013) Photochemical trapping heterogeneity as a function of wavelength in plant photosystem I (PSI-LHCI). Biochim Biophys Acta 1827:779–785

    Article  CAS  PubMed  Google Scholar 

  • Jensen PE, Bassi R, Boekema EJ, Dekker JP, Jansson S, Leister D, Robinson C, Scheller HV (2007) Structure, function and regulation of plant photosystem I. Biochim Biophys Acta 1767:335–352

    Article  CAS  PubMed  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

    Article  CAS  PubMed  Google Scholar 

  • Kaňa R (2018) Application of spectrally resolved fluorescence induction to study light-induced non-photochemical quenching in algae. Photosynthetica 56:132–138

    Article  CAS  Google Scholar 

  • Kaňa R, Kotabová E, Komárek O, Šedivá B, Papageorgiou GC, Govindjee, Prášil O (2012) The slow S to M fluorescence rise in cyanobacteria is due to a state 2 to state 1 transition. Biochim Biophys Acta 1817:1237–1247

    Article  PubMed  CAS  Google Scholar 

  • Karapetian NV (2004) Dynamics of excitation in the photosystem I of cyanobacteria: transfer in the antenna, capture by the reaction site, and dissipation. Biofizika 49:212–226

    CAS  PubMed  Google Scholar 

  • Karapetyan NV, Dorra D, Schweitzer G, Bezsmertnaya IN, Holzwarth AR (1997) Fluorescence spectroscopy of the longwave chlorophylls in trimeric and monomeric photosystem I core complexes from the cyanobacterium Spirulina platensis. Biochemistry 36:13830–13837

    Article  CAS  PubMed  Google Scholar 

  • Karukstis KK, Sauer K (1985) The effects of cation-induced and pH-induced membrane stacking on chlorophyll fluorescence decay kinetics. Biochim Biophys Acta 806:374–388

    Article  CAS  PubMed  Google Scholar 

  • Kirilovsky D, Kaňa R, Prášil O (2014) Mechanisms modulating energy arriving at reaction centers in cyanobacteria. In: Demmig-Adams B, Garab G, Adams W III, Govindjee (eds) Non-photochemical quenching and energy dissipation in plants, algae and cyanobacteria. Springer, Dordrecht, pp 471–501

    Chapter  Google Scholar 

  • Kitajima M, Butler WL (1975) Excitation spectra for photosystem I and photosystem II in chloroplasts and the spectral characteristics of the distribution of quanta between the two photosystems. Biochim Biophys Acta 408:297–305

    Article  CAS  PubMed  Google Scholar 

  • Koehne B, Trissl HW (1988) The cyanobacterium Spirulina platensis contains a long wavelength-absorbing pigment C738 (F76077K) at room temperature. Biochemistry 37:5494–5500

    Google Scholar 

  • Koehne B, Elli G, Jennings RC, Wilhelm C, Trissl HW (1999) Spectroscopic and molecular characterization of a long wavelength absorbing antenna of Ostreobium sp. Biochim Biophys Acta 1412:94–107

    Article  CAS  PubMed  Google Scholar 

  • Kok B (1956) On the reversible absorption change at 705 nm in photosynthetic organisms. Biochim Biophys Acta 22:399–401

    Article  CAS  PubMed  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Kruip J, Bald D, Boekema E, Rögner M (1994) Evidence for the existence of trimeric and monomeric photosystem I complexes in thylakoid membranes from cyanobacteria. Photosynth Res 40:279–286

    Article  CAS  PubMed  Google Scholar 

  • Kuhl M, Chen M, Ralph PJ, Schreiber U, Larkum AWD (2005) A niche for cyanobacteria containing chlorophyll d. Nature 433:820

    Article  PubMed  CAS  Google Scholar 

  • Kumazaki S, Abiko K, Ikegami I, Iwaki M, Itoh S (2002) Energy equilibration and primary charge separation in chlorophyll d-based photosystem I reaction center isolated from Acaryochloris marina. FEBS Lett 530:153–157

    Article  CAS  PubMed  Google Scholar 

  • Lamb J, Forfang K, Hohmann-Marriott M (2015) A practical solution for 77 K fluorescence measurements based on LED excitation and CCD array detector. PLoS One 10:e0132258

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Lamb JJ, Røkke G, Hohmann-Marriott MF (2018) Chlorophyll fluorescence emission spectroscopy of oxygenic organisms at 77 K. Photosynthetica 56:105–124

    Google Scholar 

  • Lathrop EJP, Friesner RA (1994) Vibronic mixing in the strong electronic coupling limit. Spectroscopic effects of forbidden transitions. J Phys Chem 98:3050–3055

    Article  CAS  Google Scholar 

  • Le Quiniou C, van Oort B, Drop B, van Stokkum IH, Croce R (2015a) The high efficiency of photosystem I in the green alga Chlamydomonas reinhardtii is maintained after the antenna size is substantially increased by the association of light-harvesting complexes II. J Biol Chem 290:30587–30595

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Le Quiniou C, Tian L, Drop B, Wientjes E, van Stokkum IHM, van Oort B, Croce R (2015b) PSI-LHCI of Chlamydomonas reinhardtii: increasing the absorption cross section without losing efficiency. Biochim Biophys Acta 1847:458–467

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Litvin FF, Sinechchekov VV (1975) Molecular organisation of chlorophyll and energetics of the initial stages in photosynethesis. In: Govindjee (ed) Bioenegetics of photosynthesis. Academi Press, New York

    Google Scholar 

  • Litvin R, Bina D, Herbstova M, Gardian Z (2016) Architecture of the light-harvesting apparatus of the eustigmatophyte alga Nannochloropsis oceanica. Photosynth Res 130:137–150

    Article  CAS  PubMed  Google Scholar 

  • Magnusson SH, Fine M, Kuhl M (2007) Light microclimate of endolithic phototrophs in the scleractinian corals Montipora monasteriata and Porites cylindrica. Mar Ecol Prog Ser 332:119–128

    Article  Google Scholar 

  • Miloslavina Y, Szczepaniak M, Muller MG, Sander J, Nowaczyk M, Rogner M, Holzwarth AR (2006) Charge separation kinetics in intact photosystem II core particles is trap-limited. A picosecond fluorescence study. Biochemistry 45:2436–2442

    Article  CAS  PubMed  Google Scholar 

  • Miyashita H, Ikemoto H, Kurano N, Adachi K, Chihara M, Miyachi S (1996) Chlorophyll d as a major pigment. Nature 383:402

    Article  CAS  Google Scholar 

  • Molotokaite E, Remelli W, Casazza AP, Zucchelli G, Polli D, Cerullo G, Santabarbara S (2017) Trapping dynamics in photosystem I-light harvesting complex I of higher plants is governed by the competition between excited state diffusion from low energy states and photochemical charge separation. J Phys Chem B 121:9816–9830

    Article  CAS  PubMed  Google Scholar 

  • Moore RB, Obornik M, Janouskovec J, Chrudimsky T, Vancova M, Green DH, Wright SW, Davies NW, Bolch CJS, Heimann K, Slapeta J, Hoegh-Guldberg O, Logsdon JM Jr, Carter DA (2008) A photosynthetic alveolate closely related to apicomplexan parasites. Nature 451:959–963

    Article  CAS  PubMed  Google Scholar 

  • Morosinotto T, Breton J, Bassi R, Croce R (2003) The nature of a chlorophyll ligand in Lhca proteins determines the far red fluorescence emission typical of photosystem I. J Biol Chem 278:49223–49229

    Article  CAS  PubMed  Google Scholar 

  • Mozzo M, Morosinotto T, Bassi R, Croce R (2006) Probing the structure of Lhca3 by mutation analysis. Biochim Biophys Acta 1757:1607–1613

    Article  CAS  PubMed  Google Scholar 

  • Murata N, Nishimura M, Takamiya A (1966) Fluorescence of chlorophyll in photosynthetic systems III. Emission and action spectra of fluorescence-three emission bands of cholophyll a and the energy transfer between two pigment systems. Biochim Biophys Acta 126:234–243

    Article  CAS  PubMed  Google Scholar 

  • Myers J, Graham J-R (1963) Enhancement in chlorella. Plant Physiol 38:105–116

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nelson N, Yocum CF (2006) Structure and function of photosystems I and II. Annu Rev Plant Biol 57:521–565

    Article  CAS  PubMed  Google Scholar 

  • Nürnberg DJ, Morton J, Santabarbara S, Telfer A, Joliot P, Antonaru LA, Ruban AV, Cardona T, Krausz E, Boussac A, Fantuzzi A, Rutherford AW (2018) Photochemistry beyond the red limit in chlorophyll f–containing photosystems. Science 360:1210–1213

    Article  PubMed  CAS  Google Scholar 

  • Nymark M, Valle KC, Hancke K, Winge P, Andresen K, Johnsen G, Bones AM, Brembu T (2013) Molecular and photosynthetic responses to prolonged darkness and subsequent acclimation to re-illumination in the diatom Phaeodactylum tricornutum. PLoS One 8:e58722

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Obornik M, Lukes J (2013) Cell biology of chromerids: autotrophic relatives to apicomplexan parasites. In: Jeon KW (ed) International review of cell and molecular biology, vol 306, pp 333–369

    Google Scholar 

  • Ohashi S, Miyashita H, Okada N, Iemura T, Watanabe T, Kobayashi M (2008) Unique photosystems in Acaryochloris marina. Photosynth Res 98:141–149

    Article  CAS  PubMed  Google Scholar 

  • Owens TG, Webb SP, Mets L, Alberte RS, Fleming GR (1987) Antenna size dependence of fluorescence decay in the core antenna of photosystem I: estimates of charge separation and energy transfer rates. Proc Natl Acad Sci U S A 84:1532–1536

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Palsson LO, Dekker JP, Schlodder E, Monshouwer R, van Grondelle R (1996) Polarised site-selected fluorescence spectroscopy of long-wavelength emitting chlorophyll in isolated photosytem I particles of Synechococcus elongates. Photosynth Res 48:239–246

    Article  CAS  PubMed  Google Scholar 

  • Pazdernik M (2015) Light harvesting complexes and chromatic adaptation of Eustigmatophyte alga Trachydiscus minutus. University of Southern Bohemia, Ceske Budejovice

    Google Scholar 

  • Pettai H, Oja V, Freiberg A, Laisk A (2005a) The long-wavelength limit of plant photosynthesis. FEBS Lett 579:4017–4019

    Article  CAS  PubMed  Google Scholar 

  • Pettai H, Oja V, Freiberg A, Laisk A (2005b) Photosynthetic activity of far-red light in green plants. Biochim Biophys Acta 1708:311–321

    Article  CAS  PubMed  Google Scholar 

  • Prášil O, Bina D, Medova H, Rehakova K, Zapomelova E, Vesela J, Oren A (2009) Emission spectroscopy and kinetic fluorometry studies of phototrophic microbial communities along a salinity gradient in solar saltern evaporation ponds of Eilat, Israel. Aquat Microb Ecol 56:285–296

    Article  Google Scholar 

  • Qin X, Suga M, Kuang T, Shen JR (2015) Photosynthesis. Structural basis for energy transfer pathways in the plant PSI-LHCI supercomplex. Science 348:989–995

    Article  CAS  PubMed  Google Scholar 

  • Quigg A, Kotabová E, Jarešova J, Kaňa R, Šetlik J, Šediva B, Komárek O, Prášil O (2012) Photosynthesis in Chromera velia represents a simple system with high efficiency. PLoS One 7:e47036

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rätsep M, Johnson TW, Chitnis PR, Small GJ (2000) The red-absorbing chlorophyll a antenna states of photosystem I: a hole-burning study of Synechocystis sp. PCC 6803 and its mutants. J Phys Chem B 104:836–847

    Article  CAS  Google Scholar 

  • Rijgersberg CP, Amesz J (1978) Changes in light absorbance and chlorophyll fluorescence in spinach choloplasts between 5 and 80°K. Biochim Biophys Acta 502:152–160

    Article  CAS  PubMed  Google Scholar 

  • Rijgersberg CP, Melis A, Amesz J, Swager JA (1979) Quenching of cholophyll fuorescence and photochemical activity of chloroplasts at low temperature in chlorophyll organization and energy transfer in photosynthesis. Ciba Foundation Symposium 61:305–322, Excerpta Medica, Amsterdam

    Google Scholar 

  • Rivadossi A, Zucchelli G, Garlaschi FM, Jennings RC (1999) The importance of PS I chlorophyll red forms in light-harvesting by leaves. Photosynth Res 60:209–215

    Article  CAS  Google Scholar 

  • Roelofs TA, Lee CH, Holzwarth AR (1992) Global target analysis of picosecond chlorophyll fluorescence kinetics from pea chloroplasts. A new approach to the characterization of the primary processes in photosystem II alfa- and beta-units. Biophys J 61:1147–1163

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Santabarbara S, Heathcote P, Evans MCW (2005) Modelling of the electron transfer reactions in photosystem I by electron tunnelling theory: the phylloquinones bound to the PsaA and the PsaB reaction centre subunits of PS I are almost isoenergetic to the iron-sulfur cluster FX. Biochim Biophys Acta 1708:283–310

    Article  CAS  PubMed  Google Scholar 

  • Santabarbara S, Agostini G, Casazza AP, Syme CD, Heathcote P, Böhles F, Evans MC, Jennings RC, Carbonera D (2007) Chlorophyll triplet states associated with photosystem I and photosystem II in thylakoids of the green alga Chlamydomonas reinhardtii. Biochim Biophys Acta 1767:88–105

    Article  CAS  PubMed  Google Scholar 

  • Santabarbara S, Tibiletti T, Remelli W, Caffarri S (2017) Kinetics and heterogeneity of energy transfer from light harvesting complex II to photosystem I in the supercomplex isolated from Arabidopsis. Phys Chem Chem Phys 19:9210–9222

    Article  CAS  PubMed  Google Scholar 

  • Schatz GH, Brock H, Holzwarth AR (1988) A kinetic and energetic model for the primary processes in photosystem II. Biophys J 54:397–405

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schellenberger Costa B, Jungandreas A, Jakob T, Weisheit W, Mittag M, Wilhelm C (2013) Blue light is essential for high light acclimation and photoprotection in the diatom Phaeodactylum tricornutum. J Exp Bot 64:483–493

    Article  CAS  PubMed  Google Scholar 

  • Schenderlein M, Çetin M, Barber J, Telfer A, Schlodder E (2008) Spectroscopic studies of the chlorophyll d containing photosystem I from the cyanobacterium Acaryochloris marina. Biochim Biophys Acta 1777:1400–1408

    Article  CAS  PubMed  Google Scholar 

  • Schubert WD, Klukas O, Saenger W, Witt HT, Fromme P, Krauss N (1998) A common ancestor for oxygenic and anoxygenic photosynthetic system: a comparison based on the structural model of photosystem I. J Mol Biol 280:297–314

    Article  CAS  PubMed  Google Scholar 

  • Searle GF, Tredwell CJ, Barber J, Porter G (1979) Picosecond time-resolved fluorescence study of chlorophyll organisation and excitation energy distribution in chloroplasts from wild-type barley and a mutant lacking chlorophyll b. Biochim Biophys Acta 545:496–507

    Article  CAS  PubMed  Google Scholar 

  • Sener MK, Lu DY, Park SH, Schulten K, Fromme P (2002) Spectral disorder and excitation transfer dynamics in cyanobacterial photosystem I. Biophys J 82:292–302

    Google Scholar 

  • Sener MK, Jolley C, Ben-Shem A, Fromme P, Nelson N, Croce R, Schulten K (2005) Comparison of the light-harvesting networks of plant and cyanobacterial photosystem I. Biophys J 89(3):1630–1642

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shimura S, Fujita Y (1973) Some properties of the chlorophyll fluorescence of the diatom Pheodactylum tricornutum. Plant Cell Physiol 14:341–352

    CAS  Google Scholar 

  • Shubin VV, Murthy SDS, Karapetyan NV, Mohanty P (1991) Origin of the 77 K variable fluorescence at 758 nm in the cyanobacterium Spirulina platensis. Biochim Biophys Acta 1060:28–36

    Article  CAS  Google Scholar 

  • Shubin VV, Tsuprun VL, Bezsmertnaya IN, Karapetyan NV (1993) Trimeric forms of the photosystem I reaction center complex pre-exist in the membranes of the cyanobacterium Spirulina platensis. FEBS Lett 334:79–82

    Article  CAS  PubMed  Google Scholar 

  • Slavov C, Ballottari M, Morosinotto T, Bassi R, Holzwarth AR (2008) Trap-limited charge separation kinetics in higher plant photosystem I complexes. Biophys J 94:3601–3612

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Thapper A, Mamedov F, Mokvist F, Hammarstrom L, Styring S (2009) Defining the far-red limit of photosystem II in spinach. Plant Cell 21:2391–2401

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tichy J, Gardian Z, Bina D, Konik P, Litvin R, Herbstova M, Pain A, Vacha F (2013) Light harvesting complexes of Chromera velia, photosynthetic relative of apicomplexan parasites. Biochim Biophys Acta 1827:723–729

    Article  CAS  PubMed  Google Scholar 

  • Tomo T, Kato Y, Suzuki T, Akimoto S, Okubo T, Noguchi T, Hasegawa K, Tsuchiya T, Tanaka K, Fukuya M, Dohmae N, Watanabe T, Mimuro M (2008) Characterization of highly purified photosystem I complexes from the chlorophyll d-dominated cyanobacterium Acaryochloris marina MBIC 11017. J Biol Chem 283:18198–18208

    Article  CAS  PubMed  Google Scholar 

  • Tumino G, Casazza AP, Engelmann ECM, Garlaschi FM, Zucchelli G, Jennings RC (2008) Fluorescence lifetime spectrum of the plant photosystem II core complex: photochemistry does not induce specific reaction center quenching. Biochemistry 47:10449–10457

    Article  CAS  PubMed  Google Scholar 

  • Turconi S, Kruip J, Schweitzer G, Rögner M, Holzwarth AR (1996) A comparative fluorescence kinetics study of photosystem I monomers and trimers from Synechocystis PCC 6803. Photosynth Res 49:263–268

    Article  CAS  PubMed  Google Scholar 

  • van Amerongen H, Croce R (2013) Light harvesting in photosystem II. Photosynth Res 116:251–263

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • van der Lee J, Bald D, Kwa SLM, van Grondelle R, Rogner M, Dekker JP (1993) Steady-state polarized-light spectroscopy of isolated photosystem-I complexes. Photosynth Res 35:311–321

    Article  PubMed  Google Scholar 

  • van Oort B, Alberts M, de Bianchi S, Dall’Osto L, Bassi R, Trinkunas G, Croce R, van Amerongen H (2010) Effect of antenna-depletion in photosystem II on excitation energy transfer in Arabidopsis thaliana. Biophys J 98:922–931

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • van Stokkum IHM, Desquilbet TE, van der Weij-de Wit CD, Snellenburg JJ, van Grondelle R, Thomas JC, Dekker JP, Robert B (2013) Energy transfer and trapping in red-chlorophyll-free photosystem I from Synechococcus WH 7803. J Phys Chem B 117:11176–11183

    Article  PubMed  CAS  Google Scholar 

  • Vernon LP, Seely GR (1966) The chlorophylls. Academic, New York City

    Google Scholar 

  • Wientjes E, Croce R (2011) The light-harvesting complexes of higher plant photosystem I: Lhca1/4 and Lhca2/3 form two red-emitting heterodimers. Biochem J 433:477–485

    Article  CAS  PubMed  Google Scholar 

  • Wientjes E, van Stokkum IHM, van Amerongen H, Croce R (2011a) Excitation-energy transfer dynamics of higher plant photosystem I light-harvesting complexes. Biophys J 100:1372–1380

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wientjes E, van Stokkum IHM, van Amerongen H, Croce R (2011b) The role of the individual Lhcas in photosystem I excitation energy trapping. Biophys J 101:745–754

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wilhelm C, Jakob T (2006) Uphill energy transfer from long-wavelength absorbing chlorophylls to PS II in Ostreobium sp. is functional in carbon assimilation. Photosynth Res 87:323–329

    Article  CAS  PubMed  Google Scholar 

  • Witt HT (1979) Energy conversion in the functional membrane of photosynthesis. Analysis by light pulse and electric pulse methods. The central role of the electric field. Biochim Biophys Acta 505:355–427

    Article  CAS  PubMed  Google Scholar 

  • Wittmershaus BP, Woolf VM, Vermaas WJF (1992) Temperature dependence and polarization of fluorescence from photosystem I in the cyanobacterium Synechocystis sp. PCC 6803. Photosynth Res 31:75–87

    Article  CAS  PubMed  Google Scholar 

  • Wolf BM, Niedzwiedzki DM, Magdaong NCM, Roth R, Goodenough U, Blankenship RE (2018) Characterization of a newly isolated freshwater Eustigmatophyte alga capable of utilizing far-red light as its sole light source. Photosynth Res 135:177–189

    Article  CAS  PubMed  Google Scholar 

  • Wollman F-A, Bennoun P (1982) A new chlorophyll-protein complex related to photosystem I in Chlamydomonas reinhardii. Biochim Biophys Acta 680:352–360

    Article  CAS  Google Scholar 

  • Yang H, Liu J, Wen X, Lu C (2015) Molecular mechanism of photosystem I assembly in oxygenic organisms. Biochim Biophys Acta 1847:838–848

    Article  CAS  PubMed  Google Scholar 

  • Zazubovich V, Matsuzaki S, Johnson TW, Hayes JM, Chitnis P, Small GJ (2003) Red antenna states of photosystem I from the cyanobacterium Synechococcus elongatus: a spectral hole burning study. Chem Phys 275:47–59

    Article  Google Scholar 

  • Zorz JK, Allanach JR, Murphy CD, Roodvoets MS, Campbell DA, Cockshutt AM (2015) The RUBISCO to photosystem II ratio limits the maximum photosynthetic rate in picocyanobacteria. Life (Basel) 5:403–417

    CAS  Google Scholar 

  • Zucchelli G, Morosinotto T, Garlaschi FM, Bassi R, Jennings RC (2005) The low energy emitting states of the Lhca4 subunit of higher plant photosystem I. FEBS Lett 579:2071–2076

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Stefano Santabarbara .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2020 Springer Nature Switzerland AG

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Santabarbara, S., Casazza, A.P., Belgio, E., Kaňa, R., Prášil, O. (2020). Light Harvesting by Long-Wavelength Chlorophyll Forms (Red Forms) in Algae: Focus on their Presence, Distribution and Function. In: Larkum, A., Grossman, A., Raven, J. (eds) Photosynthesis in Algae: Biochemical and Physiological Mechanisms. Advances in Photosynthesis and Respiration, vol 45. Springer, Cham. https://doi.org/10.1007/978-3-030-33397-3_11

Download citation

Publish with us

Policies and ethics