Skip to main content
SpringerLink
Log in

Light-Harvesting Features Revealed by the Structure of Plant Photosystem I

  • Published:
Photosynthesis Research Aims and scope Submit manuscript

Abstract

Oxygenic photosynthesis is driven by two multi-subunit membrane protein complexes, Photosystem I and Photosystem II. In plants and green algae, both complexes are composed of two moieties: a reaction center (RC), where light-induced charge translocation occurs, and a peripheral antenna that absorbs light and funnels its energy to the reaction center. The peripheral antenna of PS I (LHC I) is composed of four gene products (Lhca 1–4) that are unique among the chlorophyll a/b binding proteins in their pronounced long-wavelength absorbance and in their assembly into dimers. The recently determined structure of plant Photosystem I provides the first relatively high-resolution structural model of a super-complex containing a reaction center and its peripheral antenna. We describe some of the structural features responsible for the unique properties of LHC I and discuss the advantages of the particular LHC I dimerization mode over monomeric or trimeric forms. In addition, we delineate some of the interactions between the peripheral antenna and the reaction center and discuss how they serve the purpose of dynamically altering the composition of LHC I in response to environmental pressure. Combining structural insight with spectroscopic data, we propose how altering LHC I composition may protect PS I from excessive light.

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

References

  • Bailey S, Walters RG, Jansson S and Horton P (2001) Acclimation of Arabidopsis thaliana to the light environment: the existence of separate low light and high light responses. Planta 213: 794–801

    Article  PubMed  CAS  Google Scholar 

  • Barber J (2002) Photosystem II: a multisubunit membrane protein that oxidises water. Curr Opin Struct Biol 12: 523–530

    Article  PubMed  CAS  Google Scholar 

  • Bassi R and Simpson D (1987) Chlorophyll-protein complexes of barley photosystem I. Eur J Biochem 163: 221–230

    Article  PubMed  CAS  Google Scholar 

  • Baymann F, Brugna M, Muhlenhff U and Nitschke W (2001) Daddy, where did (PS)I come from? Biochim Biophys Acta 1507: 291–310

    Article  PubMed  CAS  Google Scholar 

  • Ben-Shem A. Frolow F and Nelson N (2003a) The crystal structure of plant Photosystem I. Nature 426: 630–635

    Article  PubMed  CAS  Google Scholar 

  • Ben-Shem A, Nelson N and Frolow F (2003b) Crystallization and initial X-ray diffraction studies of higher plant Photosystem I. Acta Cryst D59: 1824–1827

    CAS  Google Scholar 

  • Ben-Shem A, Frolow F and Nelson N (2004) Evolution of Photosystem I-From symmetry through Pseudo-symmetry to Asymmetry. FEBS Lett 564: 274–280

    Article  PubMed  CAS  Google Scholar 

  • Bengis C and Nelson N (1975) Purification and properties of the Photosystem I reaction center from chloroplasts. J Biol Chem 250: 2783–2788

    PubMed  CAS  Google Scholar 

  • Bengis C and Nelson N (1977) Subunit structure of chloroplast Photosystem I reaction center. J Biol Chem 252: 4564–4569

    PubMed  CAS  Google Scholar 

  • Bibby TS, Nield J and Barber J (2001) Iron deficiency induces the formation of an antenna ring around trimeric Photosystem I in cyanobacteria. Nature 412: 743–745

    Article  PubMed  CAS  Google Scholar 

  • Boekema EJ, Jensen PE, Schlodder E, van Breemen JF, van Roon H, Scheller HV and Dekker JP (2001) Green plant Photosystem I binds light-harvesting complex I on one side of the complex. Biochemistry 40: 1029–1036

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Büttner M, Xie D-L, Nelson H, Pinther W, Hauska G and Nelson N (1992a) Photosynthetic reaction center genes in green sulfur bacteria and in Photosystem 1 are related. Proc Natl Acad Sci USA 89: 8135–8139

    Article  PubMed  Google Scholar 

  • Büttner M, Xie D-L, Nelson H, Pinther W, Hauska G and Nelson N (1992b) The Photosystem I-like P840-reaction center of green S-bacteria is a homodimer. Biochim Biophys Acta 1101: 154–156

    PubMed  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Dedic R, Svoboda A, Psencik J, Lupinkova L, Komenda J and Hala J (2003) Time and spectral resolved phosphorescence of singlet oxygen and pigments in Photosystem II particles. J Luminesc 102-103: 313–317

    Article  CAS  Google Scholar 

  • Durnford DG, Deane JA, Tan S, McFadden GI, Gantt E and Green BR (1999) A phylogenetic assessment of the eukaryotic light-harvesting antenna proteins, with implications for plastid evolution. J Mol Evol 48: 59–68

    Article  PubMed  CAS  Google Scholar 

  • Fromme P, Melkozernov A, Jordan P and Krauss N (2003) Structure and function of Photosystem I: interaction with its soluble electron carriers and external antenna systems. FEBS Lett 555: 40–44

    Article  PubMed  CAS  Google Scholar 

  • Ganeteg U, Strand A, Gustafsson P and Jansson S (2001) The properties of the chlorophyll a/b-binding proteins Lhca2 and Lhca3 studied in vivo using antisense inhibition. Plant Physiol 127: 150–158

    Article  PubMed  CAS  Google Scholar 

  • Gobets B and van Grondelle R (2001) Energy transfer and trapping in Photosystem I. Biochim Biophys Acta 1507: 80–99

    Article  PubMed  CAS  Google Scholar 

  • Haldrup A, Simpson DJ and Scheller HV (2000) Downregulation of the PSI-F subunit of Photosystem I (PSI) in Arabidopsis thaliana. The PSI-F subunit is essential for 249 photoautotrophic growth and contributes to antenna function. J Biol Chem 275: 31211–31218

    Article  PubMed  CAS  Google Scholar 

  • Heathcote P, Jones MR and Fyfe PK (2003) Type I photosynthetic reaction centres: Form and Function. Phil Trans R Soc 358: 231–243

    Article  CAS  Google Scholar 

  • Ihalainen JA, Gobets B, Sznee K, Brazzoli M, Croce R, Bassi R, van Grondelle R, Korppi-Tommola JE and Dekker JP (2000) Evidence for two spectroscopically different dimers of light-harvesting complex I from green plants. Biochemistry 39: 8625–8631

    Article  PubMed  CAS  Google Scholar 

  • Ihalainen JA, Jensen PE, Haldrup A, van Stokkum IH, van Grondelle R, Scheller HV and Dekker JP (2002) Pigment organization and energy transfer dynamics in isolated Photosystem I (PSI) complexes from Arabidopsis thaliana depleted of the PSI-G, PSI-K, PSI-L, or PSI-N subunit. Biophys J 83: 2190–2201

    PubMed  CAS  Google Scholar 

  • Jansson S, Andersen B and Scheller HV (1996) Nearestneighbor analysis of higher-plant Photosystem I holocomplex. Plant Physiol 112: 409–420

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Jensen PE, Gilpin M, Knoetzel J and Scheller HV (2000) The PSI-K subunit of Photosystem I is involved in the interaction between light harvesting complex I-680 and the Photosystem I reaction center core. J Biol Chem 275: 24701–24708

    Article  PubMed  CAS  Google Scholar 

  • Jordan P, Fromme P, Witt HT, Klukas O, Saenger W and Krauss N (2001) Three-dimensional structure of cyanobacterial Photosystem I at 2.5 Åresolution. Nature 411: 909–917

    Article  PubMed  CAS  Google Scholar 

  • Krasnovsky AA, Lopez J, Cheng P, Liddell PA, Blankenship RE, Moore TA and Gust D (1994) Generation and quenching of singlet molecular-oxygen by aggregated bacteriochlorophyll-d in model systems and chlorosomes. Photosynth Res 40:191–198

    Article  CAS  Google Scholar 

  • Kuhlbrandt W, Wang DN and Fujiyoshi Y (1994) Atomic model of plant light-harvesting complex by electron crystallography. Nature 367: 614–621

    Article  PubMed  CAS  Google Scholar 

  • Liebl U, Mockensturm-Wilson M, Trost JT, Brune DC, Blankenship RE and Vermaas W (1993) Single core polypeptide in the reaction center of the photosynthetic bacterium Heliobacillus mobilis: structural implications and relations to other photosystems. Proc Natl Acad Sci USA 90: 7124–7128

    Article  PubMed  CAS  Google Scholar 

  • Liu Z, Yan H, Wang K, Kuang T, Zhang J, Gui L, An X and Chang W (2004) Crystal structure of spinach major light-harvesting complex at 2.72 A resolution. Nature 428: 287–292

    Article  PubMed  CAS  Google Scholar 

  • Melkozernov AN, Lin S, Bibby TS, Barber J and BlankenshipRE (2003) Time-resolved absorption and emission show that the CP43' antenna ring of iron-stressed Synechocystis sp. PCC6803 is efficiently coupled to the Photosystem I reaction center core. Biochemistry 42: 3893–3903

    Article  PubMed  CAS  Google Scholar 

  • Morosinotto T, Castelletti S, Breton J, Bassi R and Croce R (2002) Mutation analysis of Lhca1 antenna complex. Low energy absorption forms originate from pigment-pigment interactions. J Biol Chem 277: 36253–36261

    Article  PubMed  CAS  Google Scholar 

  • Morosinotto T, Breton J, Bassi R and 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  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Nelson N and Ben-Shem A (2002) Photosystem I reaction center: past and future. Photosynth Res 73: 193–206

    Article  PubMed  CAS  Google Scholar 

  • Nussberger S, Dorr K, Wang DN and Kuhlbrandt W (1993) Lipid-protein interactions in crystals of plant light-harvesting complex. J Mol Biol 234: 347–356

    Article  PubMed  CAS  Google Scholar 

  • Palsson LO, Flemming C, Gobets B, van Grondelle R, Dekker JP and Schlodder E (1998) Energy transfer and charge separation in Photosystem I: P700 oxidation upon selective excitation of the long-wavelength antenna chlorophylls of Synechococcus elongatus. Biophys J 74: 2611–2622

    Article  PubMed  CAS  Google Scholar 

  • Rivadossi A, Zucchelli G, Garlaschi FM and Jennings RC (1999) The importance of PSI chlorophyll red forms in lightharvesting by leaves. Photosynth Res 60: 209–215

    Article  CAS  Google Scholar 

  • Satoh K and Butler WL (1978) Competition between the 735 nm fluorescence and the photochemistry of Photosystem I in chloroplasts at low temperature. Biochim Biophys Acta 502: 103–110

    Article  PubMed  CAS  Google Scholar 

  • Schmid VH, Cammarata KV, Bruns BU and Schmidt GW (1997) In vitro reconstitution of the Photosystem I lightharvesting complex LHC I-730: Heterodimerization is required for antenna pigment organization. Proc Natl Acad Sci USA 94: 7667–7672

    Article  PubMed  CAS  Google Scholar 

  • Schmid VH, Paulsen H and Rupprecht J (2002) Identification of N-and C-terminal amino acids of Lhca1 and Lhca4 required for formation of the heterodimeric peripheral Photosystem I antenna LHC I-730. Biochemistry 41: 9126–9131

    Article  PubMed  CAS  Google Scholar 

  • Trissl HW and Wilhelm C (1993) Why do thylakoid membranes from higher plants form grana stacks? Trends Biochem Sci 18: 415–419

    Article  PubMed  CAS  Google Scholar 

  • Yamamoto HY and Bassi R (1996) Oxygen Photosynthesis: the Light Reactions: Carotenoids: Localization and Function. In: Ort DR and Yocumm CF (eds) Advances in Photosythesis, Vol 4, p 539. Kluwer Academic Publishers, Dordrecht, The Netherlands

    Google Scholar 

  • Zhang H, Goodman HM and Jansson S (1997) Antisense inhibition of the Photosystem I antenna protein Lhca4 in Arabidopsis thaliana. Plant Physiol 115: 1525–1531 250

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Biochemistry, The George S. Wise Faculty of Life Sciences, Tel Aviv University, Tel Aviv, 69978, Israel

    Adam Ben-Shem & Nathan Nelson

  2. Department of Molecular Microbiology and Biotechnology, The George S. Wise Faculty of Life Sciences, Tel Aviv University, Tel Aviv, 69978, Israel

    Felix Frolow

Authors
  1. Adam Ben-Shem
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Felix Frolow
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Nathan Nelson
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Adam Ben-Shem.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Ben-Shem, A., Frolow, F. & Nelson, N. Light-Harvesting Features Revealed by the Structure of Plant Photosystem I. Photosynthesis Research 81, 239–250 (2004). https://doi.org/10.1023/B:PRES.0000036881.23512.42

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/B:PRES.0000036881.23512.42

Search

Navigation