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

Summary

Membranes of bacteria, plants and animals contain carotenoid pigments as direct constituents of their lipid phase. The rod-like structure of a carotenoid molecule, often terminated with polar groups and the molecular dimensions of atypical carotenoid matching the thickness of the hydrophobic membrane core, are directly responsible for the localization and orientation of pigment molecules within the membrane and for effects on the membrane properties. Model studies have revealed several effects of carotenoids on structure and dynamics of lipid membranes. Restrictions to the motional freedom of lipids due to the hydrophobic interactions with rigid rod-like molecules of Carotenoids are the main cause of the effects on the membrane properties such as the increase in the membrane rigidity and thermostability or the increase in the penetration barrier to molecular oxygen and other small molecules. These and other effects on the membrane properties are reviewed and discussed with regard to the carotenoid biological functions in biomembranes including those already well established and experimentally proven, such as in the membranes of bacteria, those currently studied, like the effects of the xanthophyll pigments on the thylakoid membranes as well as those predictable on the basis of the results of the experiments carried out in model systems, awaiting confirmation from detailed physiological studies.

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Abbreviations

DBPC:

dibehanoylphosphatidylcholine

DGDG:

digalactosyldiacylglycerol

DLPC:

dilauroylphosphatidylcholine

DMPC:

dimyristoylphosphatidylcholine

DOPC:

dioleoylphosphatidylcholine

DPPC:

dipalmitoylphosphatidylcholine

DSPC:

distearoylphosphatidylcholine

EYPC:

egg yolk phosphatidylcholine

MGDG:

monogalactosyldiacyl-glycerol

PC:

phosphatidylcholine

SASL:

stearic acid spin label

References

  • Andersson PO, Gilbro T, Fergusson L and Cogdell RJ (1991) Absorption spectral shifts of carotenoids related to medium polarizability. Photochem Photobiol 54: 353–360

    CAS  Google Scholar 

  • Anton-Erxleben F and Langer H (1987) Dependence on carotenoids of photoreceptor ultrastructure in Spodopteria littoralis (Leodopteria, Noctuidae). Eur J Cell Biol 45: 102–106

    Google Scholar 

  • Bidigare RR, Schofield O and Prezelin BB (1989) Influence on zeaxanthin on quantum yield of photosynthesis of Synechococcus clone WH7803 (DC2). Mar Ecol Prog Ser 56:177–188

    CAS  Google Scholar 

  • Bone RA and Landrum JT (1984) Macular pigment in Henle fiber membranes: A model for Haidinger’s brushes. Vision Res 2: 103–108

    Google Scholar 

  • Bone RA, Landrum JT and Cains A (1992) Optical density spectra of the macular pigment in vivo and in vitro. Vision Res 32: 105–110

    Article  CAS  PubMed  Google Scholar 

  • Borel P, Grolier P, Armand M, Partier A, Lafont H, Lairon D and Azais-Braesco V (1996) Carotenoids in biological emulsions: solubility, surface-to-core distribution, and release from lipid droplets. J Lipid Res 37: 250–261

    CAS  PubMed  Google Scholar 

  • Britton G (1995a) UV/Visible spectroscopy. In: Britton G, Liaaen-Jensen S and Pfander H (eds) Carotenoids, Vol 1B: Spectroscopy, pp 13–62, Birkhäuser Verlag, Basel

    Google Scholar 

  • Britton G (1995b) Structure and properties of carotenoids in relation to function. FASEB J 9: 1551–1558

    CAS  PubMed  Google Scholar 

  • Brody SS (1984) Liposomes containing various carotenoids and chlorophyll: Temperature-induced changes in their spectral properties. Photobiochem Photobiobiophys 7: 205–219

    CAS  Google Scholar 

  • Chamberlain NR, Mehrtens BG, Xiong Z, Kapral FA, Boardman JL and Rearick JI (1991) Correlation ofcarotenoid production, decreased membrane fluidity, and resistance to oleic acid killing in Staphylococcus aureus 18Z. Inf Immunity 59:4332–4337

    CAS  Google Scholar 

  • Chaturvedi VK and Kurup CKR (1986) Interaction of lutein with phosphatidylcholine bilayers. Biochim Biophys Acta 860: 286–292

    CAS  Google Scholar 

  • Cruzeiri-Hansson L and Mouritsen OG (1988) Passive ion permeability of lipid membranes model via lipid-domain interfacial area. Biochim Biophys Acta 944: 63–72

    Google Scholar 

  • Edge R, McGarvey DJ and Truscott TG (1997) The carotenoids as anti-oxidants—a review. Photochem Photobiol B: Biol 41: 189–200

    CAS  Google Scholar 

  • Eskling M, Arvidsson P-O and Akerlund H-E (1997) The xanthophyll cycle, its regulation and components. Physiol Plant 100:806–816

    Article  CAS  Google Scholar 

  • Farber A and Jahns P (1998) The xanthophyll cycle of higher plants: Influence of antenna size and membrane organisation. Biochim Biophys Acta 1363: 47–58

    CAS  PubMed  Google Scholar 

  • Gabrielska J and Gruszecki WI (1996) Zeaxanthin (dihydroxy-β-carotene) but not β-carotene rigidifies lipid membranes: A 1H-N M R study of carotenoid-egg phosphatidylcholine liposomes. Biochim Biophys Acta 1285: 167–174

    CAS  PubMed  Google Scholar 

  • Gawron A, Wojtowicz K, Misiak LE and Gruszecki WI (1996) Effects of incorporation of lutein and 8-methoxypsoralen into erythrocyte and liposomal membranes. Pharmaceut Sci 2: 89–91

    CAS  Google Scholar 

  • Gombos Z and Vigh L (1986) Primary role of the cytoplasmic membrane in thermal acclimation evidenced in nitrate-starved cells of the blue-green alga, Anacystis nidulans. Plant Physiol 80: 415–419

    CAS  Google Scholar 

  • Gombos Z, Kis M, Pali T and Vigh L (1987) Nitrate starvation induces homeoviscous regulation of lipids in the cell envelope of the blue-green alga, Anacystis nidulans. Eur J Biochem 165: 461–465

    Article  CAS  PubMed  Google Scholar 

  • Grolier P, Azais-Braesco V, Zelmire L and Fessi H (1992) Incorporation of carotenoids in aqueous systems: uptake by cultured rat hepatocytes. Biochim Biophys Acta 1111: 135–138

    CAS  PubMed  Google Scholar 

  • Gruszecki WI (1986) Violaxanthin adsorption on phospholipid membranes. Stud Biophys 116: 11–18

    CAS  Google Scholar 

  • Gruszecki WI (1990a) Distribution of violaxanthin between water and lipid phases upon osmotic swelling of liposomes. Ann UMCS AAA 45: 41–44

    CAS  Google Scholar 

  • Gruszecki WI (1990b) Violaxanthin and zeaxanthin aggregation in the lipid-water system. Stud Biophys 139: 95–101

    CAS  Google Scholar 

  • Gruszecki WI (1991) Structural characterisation of the aggregated forms of violaxanthin. J Biol Physics 18: 99–109

    CAS  Google Scholar 

  • Gruszecki WI (1995) Different aspects of protective activity of the xanthophyll cycle under stress conditions. Acta Physiol Plant 17: 145–152

    CAS  Google Scholar 

  • Gruszecki WI and Krupa Z (1993) Changes of excitation spectra of in vivo chlorophyll fluorescence during induction of photosynthesis. Z Naturforsch 48c: 46–51

    Google Scholar 

  • Gruszecki WI and Sielewiesiuk J (1990) Orientation of xanthophylls in phsphatidylcholine multibilayers. Biochim Biophys Acta 1023: 405–412

    CAS  PubMed  Google Scholar 

  • Gruszecki WI and Sielewiesiuk J (1991) Galactolipid multibilayers modified with xanthophylls: orientational and diffractometric studies. Biochim Biophys Acta 1069: 21–26

    CAS  PubMed  Google Scholar 

  • Gruszecki WI and Strzalka K (1991) Does the xanthophyll cycle take part in the regulation of the fluidity of the thylakoid membrane? Biochim Biophys Acta 1060: 310–314

    CAS  Google Scholar 

  • Gruszecki WI, Smal A and Szymczuk D (1992) The effect of zeaxanthin on the thickness of dimyristoyl phosphatidylcholine bilayer: X-ray diffraction study. J Biol Physics 18: 271–280

    Google Scholar 

  • Gruszecki WI, Kernen P, Krupa Z and Strasser RJ (1994) Involvement of xanthophyll pigments in regulation of light-driven excitation quenching in light-harvesting complex of Photosystem II. Biochim Biophys Acta 1188: 235–242

    Google Scholar 

  • Gruszecki WI, Matula M, Ko-chi N, Koyama Y and Krupa Z (1997) Cis-trans-isomerization of violaxanthin in LHCII: Violaxanthin isomerization cycle within the violaxanthin cycle. Biochim Biophys Acta 1319: 267–274

    Google Scholar 

  • Hager A (1970) Formation of maxima in the absorption spectrum of carotenoids in the region around 370 nm (ger.) Planta (Berl) 91: 38–53

    CAS  Google Scholar 

  • Hager A and Holocher K (1994) Localisation of the xanthophyllcycle enzyme violaxanthin de-epoxidase within the thylakoid lumen and abolition of its mobility by a (light-dependent) pH decrease. Planta 192: 581–589

    Article  CAS  Google Scholar 

  • Havaux M and Gruszecki WI (1993) Heat-and light-induced chlorophyll a fluorescence changes in potato leaves containing high or low levels of the carotenoid zeaxanthin: Indications of a regulatory effect of zeaxanthin on thylakoid membrane fluidity. Photochem Photobiol 58: 607–614

    CAS  Google Scholar 

  • Havaux M and Tardy F (1996) Temperature-dependent adjustment of the thermal stability of Photosystem II in vivo: Possible involvement of xanthophyll-cycle pigments. Planta 193: 324–333

    Google Scholar 

  • Havaux M, Gruszecki WI, Dupont I and Leblanc RM (1991) Increased heat emission and its relationship to the xanthophyll cycle in pea leaves exposed to strong light stress. J Photochem Photobiol B: Biol 8: 361–370

    CAS  Google Scholar 

  • Havaux M, Tardy F, Ravenel J, Chanu D and Parot P (1996) Thylakoid membrane stability to heat stress studied by flash spectroscopic measurements of the electrochromic shift in intact potato leaves: Influence of the xanthophyll content. Plant Cell Environ 19: 1359–1368

    CAS  Google Scholar 

  • Huang L and Haug A (1974) Regulation of membrane lipid fluidity in Acheoplasma Laidlavi: Effect of carotenoid pigment content. Biochim Biophys Acta 352: 361–370

    CAS  PubMed  Google Scholar 

  • Huner NPA, Elfman B, Krol M and McIntosh A (1984) Growth and development at cold-hardening temperatures. Chloroplast ultrastructure, pigment content and composition. Can J Bot 62: 53–60

    CAS  Google Scholar 

  • Jahns P (1995) The xanthophyll cycle in intermittent light-grown pea plants. Plant Physiol 108: 149–156

    CAS  PubMed  Google Scholar 

  • Jezowska I, Wolak A, Gruszecki WI and Strzalka K (1994) Effet of β-carotene on structural and dynamic properties of model phosphatidylcholine membranes. II. A 31P-NMR and 13C-NMR study. Biochim Biophys Acta 1194: 143–148

    CAS  PubMed  Google Scholar 

  • Johansson LB-A, Lindblom G, Wieslander A and Arvidson G (1981) Orientation of α-carotene and retinal in lipid bilayers. FEBS Lett. 128: 97–99

    Article  CAS  Google Scholar 

  • Jürgens UJ and Mätle W (1991) Orientation of carotenoids in the outer membrane of Synechocystis PCC 6714 (cyano-bacteria). Biochim Biophys Acta 1067: 208–212

    PubMed  Google Scholar 

  • Kolev VD and Kafalieva DN (1986) Miscibility of [beta]-carotene and zeaxanthin with dipalmitoylphosphatidylcholine in multilamellar vesicles: A calorimetric and spectroscopic study. Photobiochem Photobiophys 11: 257–267

    CAS  Google Scholar 

  • Kühlbrandt W and Wang DN (1991) Three-dimensional structure of plant light-harvesting complex determined by electron crystallography. Nature 350: 130–134

    PubMed  Google Scholar 

  • Lazrak T, Milon A, Wolff G, Albrecht A-M, Miehe M, Ourisson G and Nakatani Y (1987) Comparison of the effects of inserted C40-and C50-terminally dihydroxyllated carotenoids on the mechanical properties of various phospholipid vesicles. Biochim Biophys Acta 903: 132–141

    CAS  PubMed  Google Scholar 

  • Lee AI and Thornber JP (1995) Analysis of the pigment stoichiometry of pigment-protein complexes from barley (Hordeum vulgare). Plant Physiol 107: 565–574

    Article  CAS  PubMed  Google Scholar 

  • Masamoto K and Furukawa K-I, (1997) Accumulation of zeaxanthin in cells of the cyanobacterium, Synechococcus sp. strain PCC 7942 grown under high irradiance. J Plant Physiol 151: 257–261

    CAS  Google Scholar 

  • Mendelsohn R and Van Holten RW (1979) Zeaxanthin ([3R,3′ R]-ββ-carotene-3-3 dio]) as a resonance Raman and visible absorption probe of membrane structure. Biophys J 27: 221–236

    CAS  PubMed  Google Scholar 

  • Milon A, Wolff G, Ourisson G and Nakatani Y (1986a) Organization of carotenoid-phospholipid bilayer systems. Incorporation of zeaxanthin, astaxanthin, and their C50 homologues into dimyristoyl phosphatidylcholine vesicles. Helv Chim Acta 69: 12–24

    Article  CAS  Google Scholar 

  • Milon A, Lazrak T, Albrecht A-M, Wolff G, Weill G, Ourisson G and Nakatani Y (1986b) Osmotic swelling of unilamellar vesicles by the stopped-flow light scattering method. Influence of vesicle size, solute, temperature, chloresterol and three α, ω-ihydroxycarotenoids. Biochim Biophys Acta 859: 1–9

    CAS  Google Scholar 

  • Nakagawa M and Misawa N (1991) Analysis of carotenoid glycosides produced in gram-negative bacteria by introduction of the Erwinia uredovora carotenoid biosynthesis genes. Agric Biol Chem 55: 2147–2148

    CAS  Google Scholar 

  • Omata T and Murata N (1984) Isolation and characterisation of three types of membranes from the cyanobacterium (bluegreen alga) Synechocistis PCC 6714. Arch. Microbiol. 139: 113–116

    Article  CAS  Google Scholar 

  • Pfündel E and Bilger W (1994) Regulation and possible function of the xanthophyll cycle. Photosynth Res 42: 89–109

    Article  Google Scholar 

  • Rohmer M, Bouvier P and Ourisson G (1979) Molecular evolution of biomembranes: Structural equivalents and phylogenetic precursors of sterols. Proc Natl Acad Sci USA 76: 847–851

    CAS  PubMed  Google Scholar 

  • Rottem S and Markowitz O (1979) Carotenoids acts as reinforcers of the Acholeplasma laidlawii lipid bilayer. J Bacter 140: 944–948

    CAS  Google Scholar 

  • Salares VR, Young NM, Carey PR and Bernstein HJ (1977) Excited state (exciton) interactions in polyene aggregates. Resonance Raman and absorption spectroscopic evidence. J Raman Spectr 6: 282–288

    CAS  Google Scholar 

  • Sarry J-E, Montillet J-L, Sauvaire Y and Havaux M (1994) The protective function of the xanthophyll cycle in photosynthesis. FEBS Lett 353: 147–150

    Article  CAS  PubMed  Google Scholar 

  • Schôfer C, Schmid V and Roos M (1994) Characterisation of high-light-induced increases in xanthophyll cycle pigment and lutein contents in photoautotrophic cell cultures. J Photochem Photobiol B: Biol 22: 67–75

    Google Scholar 

  • Schindler C and Lichtenthaler HK (1994) Is there a correlation between light-induced zeaxanthin accumulation and quenching of variable chlorophyll a fluorescence? Plant Physiol Biochem 32: 813–823

    CAS  Google Scholar 

  • Siefermann D and Yamamoto HY (1975) Properties of NADPH and Oxygen-dependent zeaxanthin epoxidation in isolated chloroplasts. A transmembrane model for the xanthophyll cycle. Arch Biochem Biophys 171: 70–77

    Article  CAS  PubMed  Google Scholar 

  • Siefermann-Harms D, Joyard J and Douce R (1978) Lightinduced changes of the carotenoid levels in chloroplast envelopes. Plant Physiol 61: 530–533

    CAS  Google Scholar 

  • Sielewiesiuk J, Matula M and Gruszecki WI (1997) Photooxidation of chlorophyll a in digalactosyldiacylglycerol liposomes containing xanthophyll pigments: Indication of a special photoprotective ability of zeaxanthin. Cell Mol Biol Lett 2: 59–68

    CAS  Google Scholar 

  • Strzalka K and Gruszecki WI (1994) Effect of β-carotene on structural and dynamic properties of model phosphatidylcholine membranes. I. An EPR spin label study. Biochim Biophys Acta 1194: 138–142

    CAS  PubMed  Google Scholar 

  • Strzalka K and Gruszecki WI (1997) Modulation of thylakoid membrane fluidity by exogenously added carotenoids. J Biochem Mol Biol Biophys 1: 103–108

    CAS  Google Scholar 

  • Subczynski WK, Markowska E, and Sielewiesiuk J (1991) Effect of polar carotenoids on the oxygen diffusion-concentration product in lipid bilayers. An EPR spin label study. Biochim Biophys Acta 1068: 68–72

    CAS  PubMed  Google Scholar 

  • Subczynski WK, Markowska E, Gruszecki WI and Sielewiesiuk J (1992) Effects of polar carotenoids on dimyristoyl-phosphatidylcholine membranes: A spin-label study. Biochim Biophys Acta 1105: 97–108

    CAS  PubMed  Google Scholar 

  • Subczynski WK, Markowska E and Sielewiesiuk J (1993) Biochim Biophys Acta 1150: 173–181

    Google Scholar 

  • Takagi S, Yamagami T, Takeda K and Takagi T (1987) Helical configuration of lutein aggregate dispersed in liposomes of phosphatidyl choline and digalactosyldigliceride. Agric Biol Chem 51: 1567–1572

    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 

  • Tlalka M, Gabrys H, White NS and Fricker MD (1996) Bluelight sensitive chloroplast movement. In: Senger H (ed) UV/Blue Light: Perception and Responses in Plants and Microorganisms, p 86. Phillips-Universitβt, Marburg

    Google Scholar 

  • Van de Ven M, Kattenberg M., Van Ginkel G and Levine YK (1984) Study of the orientational ordering of carotenoids in lipid bilayers by resonance-Raman spectroscopy. Biophys J 45: 1203–1210

    PubMed  Google Scholar 

  • Wisniewska A and Subczynski WK (1998) Effects of polar carotenoids on the shape of the hydrophobic barrier of phospholipid bilayers. Biochim Biophys Acta 1368: 235–246

    CAS  PubMed  Google Scholar 

  • Wojtowicz K and Gruszecki WI (1995) Effect of β-carotene, lutein and violaxanthin on structural properties of dipalmitoyl-phosphatidylcholine liposomes as studied by ultrasound absorption technique. J Biol Physics 21: 73–80

    CAS  Google Scholar 

  • Wojtowicz K, Gruszecki WI, Okulski W, Juszkiewicz, Orzechowski A and Gawda H (1991) Phase transition of zeaxanthin-modified dimyristoyl phosphatidylcholine liposomes as monitored by acoustic measurements. Stud Biophys 140: 115–120

    CAS  Google Scholar 

  • Woodall AA, Britton G and Jackson MJ (1994) Antioxidant activity of carotenoids in phosphatidylcholine vesicles: Chemical and structural considerations. Biochem Soc Trans 22: 133S

    Google Scholar 

  • Yamamoto HY and Bangham AD (1978) Carotenoid organization in membranes. Thermal transition and spectral properties of carotenoid-containing liposomes. Biochim Biophys Acta 507: 119–127

    CAS  PubMed  Google Scholar 

  • Yin J-J and Subczynski WK (1996) Effects of lutein and cholesterol on alkyl chain bending in lipid bilayers: A pulse electron spin resonance spin labelling study. Biophys J 71: 832–839

    CAS  PubMed  Google Scholar 

  • Yurkov V, Gaďon N. and Drews G (1993) The major part of polar carotenoids of the aerobic bacteria Roseococcus thiosulfatophilus RB3 and Erythromicrobium ramosum E5 is not bound to the bacteriochlorophyll α-complexes of the photosynthetic apparatus. Arch Microbiol 160: 372–376

    Article  CAS  Google Scholar 

  • Zeiger E and Zhu J (1998) Role of zeaxanthin in blue light photoreception and the modulation of light-CO2 interactions in guard cells. J Exp Botany 49: 433–442

    Article  Google Scholar 

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Gruszecki, W.I. (1999). Carotenoids in Membranes. 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_20

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  • DOI: https://doi.org/10.1007/0-306-48209-6_20

  • Publisher Name: Springer, Dordrecht

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