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Carotenoids and the Assembly of Light-harvesting Complexes

  • Chapter
The Photochemistry of Carotenoids

Part of the book series: Advances in Photosynthesis and Respiration ((AIPH,volume 8))

Summary

Carotenoids are constitutive components of all light-harvesting complexes in plants and many such complexes in bacteria. In the crystal structures of several light-harvesting complexes, carotenoids are seen to span the lipid bilayer and connect components of the complex on both membrane surfaces and/or to mediate the interaction of transmembrane protein helices. This important stabilizing function suggests that these pigments are also actively involved in the assembly of light-harvesting complexes. Verification of this notion appears too ambitious a goal at present, as the question of how the pigment-protein complexes of the photosynthetic apparatus are assembled is still open. However, information is emerging about which light-harvesting complexes depend on the presence of carotenoids during their assembly, and which carotenoids are specifically required. This information comes from experiments in which allor some carotenoids are missing during biogenesis of the photosynthetic apparatus, due either to inhibitors of carotenoid biosynthesis or mutations in carotenoid biosynthesis pathways. Further information comes from reconstitution experiments in vitro in which light-harvesting complexes are assembled from their apoproteins and a pigment mixture containing a restricted or heterologous selection of carotenoids.

One important result of such studies is that the peripheral light-harvesting complex in bacteria, LH2, but not the core antenna LH1, is dependent on carotenoids for stable assembly. The chlorophyll-a/b light-harvesting complexes in plants also assemble only when carotenoids are present. In some organisms, lutein appears to play a particularly important role: when lutein is missing, at least some of the chlorophyll-a/b complexes do not assemble. On the other hand, in other organisms the lack of lutein has no obvious effect on the chlorophyll-a/b antenna. An explanation may come from in-vitro reconstitution experiments: light-harvesting complexes in which luteins presumably are replaced with other carotenoids exhibit lower stabilities than those reconstituted with the authentic pigment, and different organisms may vary in their ability to tolerate this reduced complex stability.

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Abbreviations

BChl:

bacteriochlorophyll

Chl:

chlorophyll

CP29, CP26, and CP24:

pigment complexes of Lhcb4, Lhcb5, and Lhcb6, respectively

LH1 and LH2-bacterial:

light-harvesting complexes 1 and 2, respectively

LHCI and LHCII:

plant light-harvesting complexes of Photosystems I and II, respectively

Major LHCII:

pigment complex of Lhcb1 and Lhcb2

References

  • Adamska I (1997) Elips: Light induced stress proteins. Physiol Plant 100: 794–805

    Article  CAS  Google Scholar 

  • Bassi R, Pineau B, Dainese P and Marquardt J (1993) Carotenoid-binding proteins of Photosystem II. Eur J Biochem 212: 297–303

    Article  CAS  PubMed  Google Scholar 

  • Bishop NI (1996) The βε carotenoid, lutein, is specifically required for the formation of the oligomeric forms of the light harvesting complex in the green alga, Scenedesmus obliquus. J Photochem Photobiol B Biol 36: 279–283

    CAS  Google Scholar 

  • Bishop NI, Urbig T and Senger H (1995) Complete separation of the βε and ββ-carotenoid biosynthetic pathways by a unique mutation of the lycopene cyclase in the green alga, Scenedesmus obliquus. FEBS Lett 367: 158–162

    Article  CAS  PubMed  Google Scholar 

  • Booth PJ and Paulsen H (1996) Assembly of light-harvesting chlorophyll a/b complex in vitro. Time-resolved fluorescence measurements. Biochemistry 35: 5103–5108

    CAS  PubMed  Google Scholar 

  • Booth PJ, Riley ML, Flitsch SL, Templer RH, Farooq A, Curran AR, Chadborn N and Wright P (1997) Evidence that bilayer bending rigidity affects membrane protein folding. Biochemistry 36: 197–203

    Article  CAS  PubMed  Google Scholar 

  • Brand M and Drews G (1997) The role of pigments in the assembly of photosynthetic complexes in Rhodobacter capsulatus. J Basic Microbiol 37: 235–244

    CAS  Google Scholar 

  • Cammarata KV and Schmidt GW (1992) In-vitro reconstitution of a light-harvesting gene product—deletion mutagenesis and analyses of pigment binding. Biochemistry 31: 2779–2789

    Article  CAS  PubMed  Google Scholar 

  • Cogdell RJ, Fyfe PK, Barrett SJ, Prince SM, Freer AA, Isaacs NW, Mcglynn P and Hunter CN (1996) The purple bacterial photosynthetic unit. Photosynth Res 48: 55–63

    Article  CAS  Google Scholar 

  • Dahlin C (1993) Import of nuclear-encoded proteins into carotenoid-deficient young etioplasts. Physiol Plant 87: 410–416

    Article  CAS  Google Scholar 

  • Dahlin C and Franzén LG (1997) Carotenoid deficient young wheat etioplasts are able to bind precursor proteins on the plastid surface but are impaired in their translocation ability. Physiol Plant 99: 279–285

    Article  CAS  Google Scholar 

  • Dahlin C and Timko MP (1994) Integration of nuclear-encoded proteins into pea thylakoids with different pigment contents. Physiol Plant 91: 212–218

    Article  CAS  Google Scholar 

  • Davis CM, Bustamante PL and Loach PA (1995) Reconstitution of the bacterial core light-harvesting complexes of Rhodobacler sphaeroides and Rhodospirillum rubrum with isolated alpha-and beta-polypeptides, bacteriochlorophyll a, and carotenoid. J Biol Chem 270: 5793–5804

    Article  CAS  PubMed  Google Scholar 

  • Eichenberger W, Boschetti A and Michel HP (1986) Lipid and pigment composition of a chlorophyll b-deficient mutant of Chlamydomonas reinhardttii. Physiol Plant 66: 589–594

    CAS  Google Scholar 

  • Ermler U, Fritzsch G, Buchanan SK and Michel H (1994) Structure of the photosynthetic reaction centre from Rhodobacter sphaeroides at 2,65 Å resolution: Cofactors and protein-cofactor interactions. Structure 2: 925–936

    Article  CAS  PubMed  Google Scholar 

  • Foidl M, Golecki JR and Oelze J (1997) Phototrophic growth and chlorosome formation in Chloroflexus aurantiacus under conditions of carotenoid deficiency. Photosynth Res 54: 219–226

    Article  CAS  Google Scholar 

  • Frese R, Oberheide U, van Stokkum I, van Grondelle R, Foidl M, Oelze J and van Amerongen H (1997) The organization of bacteriochlorophyll c in chlorosomes from Chloroflexus aurantiacus and the structural role of carotenoids and protein—An absorption, linear dichroism, circular dichroism and Stark spectroscopy study. Photosynth Res 54: 115–126

    Article  CAS  Google Scholar 

  • Funk C, Schröder WP, Napiwotzki A, Tjus SE, Renger G and Andersson B (1995) The PS II-S protein of higher plants: A new type of pigment-binding protein. Biochemistry 34: 11133–11141

    Article  CAS  PubMed  Google Scholar 

  • Giuffra E, Cugini D, Croce R and Bassi R (1996) Reconstitution and pigment-binding properties of recombinant CP29. Eur J Biochem 238: 112–120

    Article  CAS  PubMed  Google Scholar 

  • Griffith DE and Stanier RY (1956) Some mutagene changes in the photosynthetic system of Rhodpseudomonas sphaeroides. J Gen Microbiol 14: 698–715

    Google Scholar 

  • Havaux M (1998) Carotenoids as membrane stabilizers in chloroplasts. Trends Plant Sci 3: 147–151

    Google Scholar 

  • Heinze I, Pfündel E, Huhn M and Dau H (1997) Assembly of light harvesting complexes II(LHC II) in the absence of lutein: A study on the alpha carotenoid free mutant C 2a′ 34 of the green alga Scenedesmus obliquus. Biochim Biophys Acta 1320: 188–194

    CAS  Google Scholar 

  • Herrin DL, Battey JF, Greer K and Schmidt GW (1992) Regulation of chlorophyll apoprotein expression and accumulation — requirements for Carotenoids and chlorophyll. J Biol Chem 267: 8260–8269

    CAS  PubMed  Google Scholar 

  • Hobe S, Prytulla S, Kühlbrandt W and Paulsen H (1994) Trimerization and crystallization of reconstituted light-harvesting chlorophyll a/b complex. EMBO J 13: 3423–3429

    CAS  PubMed  Google Scholar 

  • Hofmann E, Wrench PM, Sharpies FP, Hiller RG, Welte W and Diederichs K (1996) Structural basis of light harvesting by Carotenoids: Peridinin-chlorophyll-protein from Amphidinium carterae. Science 272: 1788–1791

    CAS  PubMed  Google Scholar 

  • Humbeck K, Römer S and Senger H (1989) Evidence for an essential role of carotenoids in the assembly of an active Photosystem II. Planta 179: 242–250

    Article  CAS  Google Scholar 

  • Hunter CN, Hundle BS, Hearst JE, Lang HP, Gardiner AT, Takaichi S and Cogdell RJ (1994) Introduction of new carotenoids into the bacterial photosynthetic apparatus by combining the carotenoid biosynthetic pathways of Erwinia herbicola and Rhodobacter sphaeroides. J Bacteriol 176: 3692–3697

    CAS  PubMed  Google Scholar 

  • Hurry V, Anderson JM, Chow WS and Osmond CB (1997) Accumulation of zeaxanthin in abscisic acid deficient mutants of Arabidopsis does not affect chlorophyll fluorescence quenching or sensitivity to photoinhibition in vivo. Plant Physiol 113: 639–648

    CAS  PubMed  Google Scholar 

  • Jahns P and Schweig S (1995) Energy-dependent fluorescence quenching in thylakoids from intermittent light grown pea plants: Evidence for an interaction of zeaxanthin and the chlorophyll a/b binding protein CP26. Plant Physiol Biochem 33: 683–687

    CAS  Google Scholar 

  • Jansson S (1994) The light-harvesting chlorophyll a/b binding proteins. Biochim Biophys Acta 1184: 1–19

    CAS  PubMed  Google Scholar 

  • Jirsakova V and Reiss-Husson F (1994) A specific carotenoid is required for reconstitution of the Rubrivivax gelatinosus B875 light harvesting complex from its subunit form B820. FEBS Lett 353: 151–154

    Article  CAS  PubMed  Google Scholar 

  • Karrasch S, Bullough PA and Ghosh R (1995) The 8.5 Å projection map of the light-harvesting complex I from Rhodospirillum rubrum reveals a ring composed of 16 subunits. EMBO J 14: 631–638

    CAS  PubMed  Google Scholar 

  • Kerfeld CA, Yeates TO and Thornber JP (1994) Biochemical and spectroscopic characterization of the reaction center LH1 complex and the carotenoid-containing B820 subunit of Chromatium purpuratum. Biochim Biophys Acta 1185: 193–202

    CAS  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Kuki M, Nagae H, Cogdell RJ, Shimada K and Koyama Y (1994) Solvent effect on spheroidene in nonpolar and polar solutions and the environment of spheroidene in the light-harvesting complexes of Rhodobacter sphaeroides 2.4.1 as revealed by the energy of the 1A −g →1B +u absorption and the frequencies of the vibronically couple C=C stretching Raman lines in the 1A −b and 21A −b states. Photochem Photobiol 59: 116–124

    CAS  Google Scholar 

  • Kuttkat A, Edhofer 1, Eichacker LA and Paulsen H (1997) Light harvesting chlorophyll a/b binding protein stably inserts into etioplast membranes supplemented with Zn pheophytin a/b. J Biol Chem 272: 20451–20455

    Article  CAS  PubMed  Google Scholar 

  • Lancaster CRD and Michel H (1996) Three-dimensional structures of photosynthetic reaction centers. Photosynth Res 48: 65–74

    Article  CAS  Google Scholar 

  • Lang HP and Hunter CN (1994) The relationship between carotenoid biosynthesis and the assembly of the light-harvesting LH2 complex in Rhodobacter sphaeroides. Biochem J 298: 197–205

    CAS  PubMed  Google Scholar 

  • Lindahl M, Funk C, Webster J, Bingsmark S, Adamska I and Andersson B (1997) Expression of ELIPs and PS II-S protein in spinach during acclimative reduction of the Photosystem II antenna in response to increased tight intensities. Photosynth Res 54: 227–236

    Article  CAS  Google Scholar 

  • Loach PA, Parkes-Loach PS, Davis CM and Heller BA (1994) Probing protein structural requirements for formation of the core light-harvesting complex of photosynthetic bacteria using hybrid reconstitution methodology. Photosynth Res 40: 231–245

    Article  CAS  Google Scholar 

  • Markgraf T and Oelmüller R (1991) Evidence that carotenoids are required for the accumulation of a functional photosystem-II, but not photosystem-I in the cotyledons of mustard seedlings. Planta 185: 97–104

    Article  CAS  Google Scholar 

  • McDermott G, Prince SM, Freer AA, Hawthornthwaite-Lawless AM, Papiz MZ, Cogdell RJ and Isaacs NW (1995) Crystal structure of an integral membrane light-harvesting complex from photosynthetic bacteria. Nature 374: 517–521

    Article  CAS  Google Scholar 

  • Meyer M and Wilhelm C (1993) Reconstitution of light-harvesting complexes from Chlorella fusca (Chlorophyceae) and Mantoniella squamata (Prasinophyceae). Z Naturforsch C 48: 461–473

    CAS  Google Scholar 

  • Moskalenko AA and Karapetyan NV (1996) Structural role of carotenoids in photosynthetic membranes. Z Naturforsch C 51: 763–771

    CAS  Google Scholar 

  • Olson JM (1998) Chlorophyll organization and function in green photosynthetic bacteria. Photochem Photobiol 67: 61–75

    Article  CAS  Google Scholar 

  • Niyogi KK, Bjorkman O and Grossman AR (1997a) Chlamydomonas xanthophyll cycle mutants identified by video imaging of chlorophyll fluorescence quenching. Plant Cell 9: 1369–1380

    Article  CAS  PubMed  Google Scholar 

  • Niyogi KK, Bjorkman O and Grossman AR (1997b) The roles of specific xanthophylls in photoprotection. Proc Natl Acad Sci USA 94: 14162–14167

    Article  PubMed  Google Scholar 

  • Oberlé B, Tichy HV, Hornberger U & Drews G (1990) Regulation of formation of photosynthetic light-harvesting complexes in Rhodobacler capsulatus. In: Drews G and Dawes EA (eds) Molecular Biology of Membrane-Bound Complexes in Phototrophic Bacteria, pp. 77–84. Plenum Press, New York.

    Google Scholar 

  • Park H and Hoober JK (1997) Chlorophyll synthesis modulates retention of apoproteins of light-harvesting complex II by the chloroplast in Chlamydomonas reinhardtii. Physiol Plant 101: 135–142

    Article  CAS  Google Scholar 

  • Paulsen H (1997) Pigment ligation to proteins of the photosynthetic apparatus in higher plants. Physiol Plant 100: 760–768

    Article  CAS  Google Scholar 

  • Paulsen H, Rümler U and Rüdiger W (1990) Reconstitution of pigment-containing complexes from light-harvesting chlorophyll a/b-binding protein overexpressed in E. coli. Planta 181: 204–211

    CAS  Google Scholar 

  • Paulsen H, Finkenzeller B and Kühlein N (1993) Pigments induce folding of light-harvesting chlorophyll a/b-binding protein. Eur J Biochem 215: 809–816

    Article  CAS  PubMed  Google Scholar 

  • Phillip D and Young AJ (1995) Occurrence of the carotenoid lactucaxanthin in higher plant LHC II. Photosynth Res 43: 273–282

    Article  CAS  Google Scholar 

  • Pichersky E and Jansson S (1996) The light-harvesting chlorophyll a/b-binding polypeptides and their genes in angiosperm and gymnosperm species. In: Ort DR and Yocum CF (eds) Oxygenic Photosynthesis: The Light Reactions, pp. 507–521. Kluwer Academic Publishers, Dordrecht

    Google Scholar 

  • Plumley FG and Schmidt GW (1995) Light-harvesting chlorophyll a/b complexes: Interdependent pigment synthesis and protein assembly. Plant Cell 7: 689–704

    Article  CAS  PubMed  Google Scholar 

  • Plumley FG and Schmidt GW (1987) Reconstitution of chlorophyll a/b light-harvesting complexes: Xanthophyll-dependent assembly and energy transfer. Proc Natl Acad Sci USA 84: 146–150

    CAS  Google Scholar 

  • Pogson B, McDonald KA, Truong M, Britton G and DellaPenna D (1996) Arabidopsis carotenoid mutants demonstrate that lutein is not essential for photosynthesis in higherplants. Plant Cell 8: 1627–1639

    Article  CAS  PubMed  Google Scholar 

  • Popot JL (1993) Integral membrane protein structure: Transmembrane alpha-helices as autonomous folding domains. Curr Opin Struct Biol 3: 532–540

    Article  CAS  Google Scholar 

  • Popot JL and Engelman DM (1990) Membrane protein folding and oligomerization: The two-stage model. Biochemistry 29: 4031–4037

    Article  CAS  PubMed  Google Scholar 

  • Rhee KH, Morris EP, Zheleva D, Hankamer B, Kühlbrandt W and Barber J (1997) Two dimensional structure of plant Photosystem II at 8 Å resolution. Nature 389: 522–526

    CAS  Google Scholar 

  • Rock CD and Zeevaart JAD (1991) The aba mutant of Arabidopsis thaliana is impaired in epoxy-carotenoid biosynthesis. Proc Natl Acad Sci USA 88: 7496–7499

    CAS  PubMed  Google Scholar 

  • Rock CD, Bowlby NR, Hoffmann-Benning S and Zeevaart JAD (1992) The aba mutant of Arabidopsis thaliana (L) Heynh. has reduced chlorophyll fluorescence yields and reduced thylakoid stacking. Plant Physiol 100: 1796–1801

    CAS  Google Scholar 

  • Römer S, Humbeck K and Senger H (1990) Relationship between biosynthesis of carotenoids and increasing complexity of Photosystem I in mutant C-6D of Scenedesmus obliquus. Planta 182: 216–222

    Article  Google Scholar 

  • Römer S, Senger H and Bishop NI (1995) Characterization of the carotenoidless strain of Scenedesmus obliquus, mutant C-6E, a living Photosystem I model. Bot Acta 108: 80–86

    Google Scholar 

  • Ros F, Bassi R and Paulsen H (1998) Pigment binding properties of the recombinant Photosystem II subunit CP26 reconstituted in vitro. Eur J Biochem, in press

    Google Scholar 

  • Ruban AV, Young AJ and Morton P (1996) Dynamic properties of the minor chlorophyll a/b binding proteins of Photosystem II, an in vitro model for photoprotective energy dissipation in the photosynthetic membrane of green plants. Biochemistry 35: 674–678

    Article  CAS  PubMed  Google Scholar 

  • Ruban AV, Phillip D, Young AJ and Horton P (1997) Carotenoid dependent oligomerization of the major chlorophyll a/b light harvesting complex of Photosystem II of plants. Biochemistry 36: 7855–7859

    Article  CAS  PubMed  Google Scholar 

  • Sandmann G (1994) Carotenoid biosynthesis in microorganisms and plants. Eur J Biochem 223: 7–24

    Article  CAS  PubMed  Google Scholar 

  • Sandmann G, Bishop NI and Senger H (1997) The carotenoid deficient mutant, C 6E, of Scenedesmus obliquus is blocked at the site of phytoene synthase. Physiol Plant 99: 391–394

    Article  CAS  Google Scholar 

  • Schmid VHR, Cammarata KV, Bruns BU and Schmidt GW (1997) In vitro reconstitution of the Photosystem I light harvesting complex LHCI 730: Heterodimerization is required for antenna pigment organization. Proc Nat. Acad Sci USA 94: 7667–7672

    CAS  PubMed  Google Scholar 

  • Tardy F and Havaux M (1996) Photosynthesis, chlorophyll fluorescence, light-harvesting system and photoinhibition resistance of a zeaxanthin-accumulating mutant of Arabidopsis thaliana. J Photochem Photobiol B-Biol 34: 87–94

    CAS  Google Scholar 

  • Tardy F and Havaux M (1997) Thylakoid membrane fluidity and thermostability during the operation of the xanthophyll cycle in higher-plant chloroplasts. Biochim Biophys Acta 1330: 179–193

    CAS  PubMed  Google Scholar 

  • Trebst A and Depka B (1997) Role of carotene in the rapid turnover and assembly of Photosystem II in Chlamydomonas reinhardtii. FEBS Lett 400: 359–362

    Article  CAS  PubMed  Google Scholar 

  • Visschers RW, Nunn R, Calkoen F, van Mourik F, Hunter CN, Rice DR and van Grondelle R (1992) Spectroscopic characterization of B820 subunits from light-harvesting complex I of Rhodospirillum rubrum and Rhodobacter sphaeroides prepared with the detergent n-octyl-rac-2,3-dipropyl-sulfoxide. Biochim Biophys Acta 1100: 259–266

    CAS  Google Scholar 

  • Wolfe GR, Park H, Sharp WP and Hoober JK (1997) Light harvesting complex apoproteins in cytoplasmic vacuoles in Chlamydomonas reinhardtii (Chlorophyta). J Phycol 33: 377–386

    Article  Google Scholar 

  • Zurdo J, Centeno MA, Odriozola JA, Fernandez-Cabrera C and Ramirez JM (1995) The structural role of the carotenoid in the bacterial light-harvesting protein 2 (LH2) of Rhodobacter capsulatus. A Fourier transform Raman spectroscopy and circular dichroism study. Photosynth Res 46: 363–369

    Article  CAS  Google Scholar 

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Authors and Affiliations

  1. Institut für Allgemeine Botanik der Universität Mainz, Müllerweg 6, D-55099, Mainz, Germany

    Harald Paulsen

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  1. Harald Paulsen
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  1. University of Connecticut, Storrs, CT, USA

    Harry A. Frank

  2. Liverpool John Moores University, Liverpool, UK

    Andrew J. Young

  3. University of Liverpool, Liverpool, UK

    George Britton

  4. University of Glasgow, Glasgow, UK

    Richard J. Cogdell

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Paulsen, H. (1999). Carotenoids and the Assembly of Light-harvesting Complexes. In: Frank, H.A., Young, A.J., Britton, G., Cogdell, R.J. (eds) The Photochemistry of Carotenoids. Advances in Photosynthesis and Respiration, vol 8. Springer, Dordrecht. https://doi.org/10.1007/0-306-48209-6_7

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