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Biochemistry and Molecular Biology of the Xanthophyll Cycle

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The Photochemistry of Carotenoids

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

Summary

The xanthophyll cycle is the cyclical interconversion of violaxanthin, antheraxanthin and zeaxanthin in plants and green algae. The existence of the cycle has been known for many years but has attracted renewed interest because of its role in protection of plants against the potentially harmful effects of excess light by enhancing the dissipation of excess energy as heat. The cycle is catalyzed by two enzymes that are localized on opposite sides of the thylakoid membrane. The de-epoxidase that converts violaxanthin to zeaxanthin by way of the intermediate, antheraxanthin, is localized in the thylakoid lumen. The epoxidase that catalyzes the resynthesis of violaxanthin is bound to the stromal side of the membrane. The extent and rate of zeaxanthin and antheraxanthin formation (de-epoxidation) are affected by at least four factors, namely, (i) pool size, (ii) availability, (iii) ascorbate, and (iv) lumen pH. The mechanism for de-epoxidation is assumed to be reduction followed by dehydration. Factors affecting the recovery of violaxanthin (epoxidation) include levels of NADPH, ferredoxin, ferredoxin-oxidoreductase and FAD. The mechanism of epoxidation is assumed to be similar to other monooxygenases wherein hydroperoxyflavin is involved and one oxygen atom from molecular oxygen is incorporated. Recently, the cDNAs for both enzymes were isolated and catalytic activities of the expressed proteins demonstrated. Analyses of the deduced polypeptide sequences indicate that both proteins belong to the lipocalin family. The lipocalins are a diverse group of proteins with a conserved barrel structure that bind small hydrophobic molecules. This chapter summarizes the biochemistry of the xanthophyll cycle and examines recent advances in the molecular biology of the cycle.

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Abbreviations

A:

antheraxanthin

ABA:

abscisic acid

CaMV:

cauliflower mosaic virus

D:

diatoxanthin

DGDG:

digalactosyldiacylglyceride

DTT:

dithiothreitol

Elips:

early isoelectric focusing

IML:

intermittent light

LHC:

light-harvesting complex

LCHI:

light-harvesting complex of Photosystem 1

LHCII:

light-harvesting complex of Photosystem 11

MGDG:

monogalactosyldiacylglyceride

NPQ:

non-photochemical quenching

PFD:

photon-flux density

V:

violaxanthin

VDE:

violaxanthin de-epoxidase

Z:

zeaxanthin

ZE:

zeaxanthin epoxidase

References

  • Adams WW III and Demmig-Adams B (1995) The xanthophyll cycle and sustained thermal energy dissipation activity in Vinca minor and Euonymus kiautschovicus in winter. Plant Cell Environ 18: 117–127

    Google Scholar 

  • Åkerlund H-E, Arvidsson P-O, Bratt CE and Carlsson M (1995) Partial purification of the violaxanthin de-epoxidase. In: Mathis P (ed) Photosynthesis From Light to Biosphere, Vol. IV, pp 103–106. Kluwer Academic Publishers, Dordrecht

    Google Scholar 

  • Arvidsson P-O, Bratt CE, Carlsson M and Åkerlund H-E (1996) Purification and identification of the violaxanthin de-epoxidase as a 43 kDa protein. Photosynth Res 49: 119–129

    Article  CAS  Google Scholar 

  • Arvidsson P-O, Carlsson M, Stefánsson H, Albertsson P-Å and Åkerlund H-E (1997) Violaxanthin accessibility and temperature dependency for de-epoxidation in spinach thylakoid membranes. Photosynth Res 52: 39–48

    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 

  • Bilger W and Björkman O (1991) Temperature dependence of violaxanthin de-epoxidation and non-photochemical fluorescence quenching in intact leaves of Gossypium hirsutum L. and Malva parviflora L. Planta 184:226–234

    CAS  Google Scholar 

  • Bilger W, Fisahn J, Brummet W, Kossmann J and Willmitzer L (1995) Violaxanthin cycle pigment contents in potato and tobacco plants with genetically reduced photosynthetic capacity. Plant Physiol 108:1479–1486

    CAS  PubMed  Google Scholar 

  • Bouvier F, ďHarlingue A, Hugueney P, Marin E, Marion-Poll A and Camara B (1996) Xanthophyll biosynthesis: Cloning, expression, functional reconstitution, and regulation of β-cyclohexenyl carotenoid epoxidase from pepper (Capsicum annuum). J Biol Chem 271: 28861–28867

    CAS  PubMed  Google Scholar 

  • Bratt CE, Arvidsson P-O, Carlsson M and Åkerlund H-E (1995) Regulation of violaxanthin de-epoxidase activity by pH and ascorbate concentration. Photosynth Res 45: 169–175

    Article  CAS  Google Scholar 

  • Büch K, Stransky H and Hager A (1995) FAD is a further essential cofactor of the NAD(P)H and O2-dependent zeaxanthin-epoxidase. FEBS Lett 376: 45–48

    Article  PubMed  Google Scholar 

  • Bugos RC and Yamamoto HY (1996) Molecular cloning of violaxanthin de-epoxidase from romaine lettuce and expression in Escherichia coli. Proc Natl Acad Sci USA 93: 6320–6325

    Article  CAS  PubMed  Google Scholar 

  • Bugos RC, Hieber AD and Yamamoto HY (1998) Xanthophyll-cycle enzymes are members of the lipocalin family, the first identified from plants. J Biol Chem 273: 15321–15324

    Article  CAS  PubMed  Google Scholar 

  • Burbidge A, Grieve T, Terry C, Corlett J, Thompson A and Taylor I (1997) Structure and expression of a cDNA encoding zeaxanthin epoxidase, isolated from a wilt-related tomato (Lycopersicon esculentum Mill.) library. J Exp Bot 48: 1749–1750

    CAS  Google Scholar 

  • Demmig-Adams B and Adams WW III (1996) The role of Xanthophyll cycle carotenoids in the protection of photosynthesis. Trends Plant Sci 1: 21–26

    Google Scholar 

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

    Article  CAS  Google Scholar 

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

    PubMed  Google Scholar 

  • Flower, DR (1996) The lipocalin protein family: Structure and function. Biochem J 318: 1–14

    CAS  PubMed  Google Scholar 

  • Frank HA, Cua A, Chynwat V, Young A, Gosztola D and Wasielewski MR (1994) Photophysics of the carotenoids associated with the xanthophyll cycle in photosynthesis. Photosyn Res 41: 389–395

    CAS  Google Scholar 

  • Gilmore AM (1997) Mechanistic aspects of xanthophyll cycledependent photoprotection in higher plant chloroplasts and leaves. Physiol Plant 99: 197–209

    Article  CAS  Google Scholar 

  • Gilmore AM and Yamamoto HY (1991) Resolution of lutein and zeaxanthin using a non-endcapped, lightly carbon-loaded C18 high-performance liquid chromatographic column. J Chromatogr 543: 137–145

    Article  CAS  Google Scholar 

  • Gilmore AM, Mohanty N and Yamamoto HY (1994) Epoxidation of zeaxanthin and antheraxanthin reverses non-photochemical quenching of photosystem II chlorophyll a fluorescence in the presence of trans-thylakoid ΔpH. FEBS Lett 350: 271–274

    Article  CAS  PubMed  Google Scholar 

  • Gilmore AM, Hazlett TL and Govindjee (1995) Xanthophyll cycle-dependent quenching of Photosystem II chlorophyll a fluorescence: Formation of a quenching complex with a short fluorescence lifetime. Proc Natl Acad Sci USA 92:2273–2277

    CAS  PubMed  Google Scholar 

  • Gilmore AM, Hazlett TL, Debrunner PG and Govindjee (1996) Photosystem II chlorophyll a fluorescence lifetimes and intensity are independent of the antenna size differences between barley wild-type and chlorina mutants: Photochemical quenching and xanthophyll cycle-dependent nonphotochemical quenching of fluorescence. Photosynth Res 48:171–187

    Article  CAS  Google Scholar 

  • Gruszecki WI and Krupa Z (1993) LHCII, the major light-harvesting pigment-protein complex, is a zeaxanthin epoxidase. Biochim Biophys Acta 1144: 97–101

    CAS  Google Scholar 

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

    Google Scholar 

  • Hager A (1969) Lichtbedingte pH-erniedrigung in einem chloroplasten-kompartiment als ursache der enzymatischen violaxanthin → zeaxanthin-umwandlung: beziehungen zur photophosphorylierung. Planta 89: 224–243

    Article  CAS  Google Scholar 

  • Hager A (1975) Die reversiblen, lichtabhängigen xanthophyllumwandlungen im chloroplasten. Ber Deutsch Bot Ges Bd 88: 27–44

    CAS  Google Scholar 

  • Hager A and Holocher K (1994) Localization of the xanthophyll-cycle 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 

  • Hager A and Perz H (1970) Veränderung der lichtabsorption eines carotinoids im enzym (de-epoxidase)-substrat(viola-xanthin)-komplex. Planta 93: 314–322

    Article  CAS  Google Scholar 

  • Hager A and Stransky H (1970) Das carotinoidmuster und die verbreitung des lichtinduzierten xanthophyll-cyclus in verschiedenen algenklassen V. Einzelne vertreter der Cryptophyceae, Euglenophyceae, Bacillariophyceae, Chrysophyceae und Phaeophyceae. Archiv Mikrobiol 73: 77–89

    Article  CAS  Google Scholar 

  • Härtel H, Lokstein H, Grimm B and Rank B (1996) Kinetic studies on the xanthophyll cycle in barley leaves: Influence of antenna size and relations to nonphotochemical chlorophyll fluorescence quenching. Plant Physiol 110: 471–482

    PubMed  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 198: 324–333

    Article  CAS  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 (1995) The xanthophyll cycle in intermittent light-grown pea plants: Possible functions of chlorophyll a/b-binding proteins. Plant Physiol 108: 149–156

    CAS  PubMed  Google Scholar 

  • Jahns P and Miehe B (1996) Kinetic correlation of recovery from photoinhibition and zeaxanthin epoxidation. Planta 198: 202–210

    Article  CAS  Google Scholar 

  • Jandrositz A, Turnowsky F and Högenauer G (1991) The gene encoding squalene epoxidase from Saccharomyces cerevisiae: cloning and characterization. Gene 107: 155–160

    Article  CAS  PubMed  Google Scholar 

  • Koornneef M, Jorna ML, Brinkhorst-van der Swan DLC and Karssen CM (1982) The isolation of abscisic acid (ABA) deficient mutants by selection of induced revertants in nongerminating gibberellin sensitive lines of Arabidopsis thaliana (L.) Heynh. Theor Appl Genet 61: 385–393

    CAS  Google Scholar 

  • Król M, Sprangfort MD, Huner NPA, Öquist G, Gustafsson P and Jansson S (1995) Chlorophyll a/b-binding proteins, pigment conversions, and early light-induced proteins in a chlorophyll b-less barley mutant. Plant Physiol 107: 873–883

    PubMed  Google Scholar 

  • Levy H, Tamar T, Shaish A and Zamir A (1993) Cbr, an algal homolog of plant early light-induced proteins, is a putative zeaxanthin binding protein. J Biol Chem 268: 20892–20896

    CAS  PubMed  Google Scholar 

  • Logan BA, Barker DH, Demmig-Adams B and Adams WW III (1996) Acclimat ion of leaf carotenoid composition and ascorbate levels to gradients in the light environment within an Australian rain forest. Plant Cell Environ 19: 1083–1090

    CAS  Google Scholar 

  • Lukowitz W, Mayer U and Jürgens G (1996) Cytokinesis in the Arabidopsis embryo involves the syntaxin-related KNOLLE gene product. Cell 84: 61–71

    Article  CAS  PubMed  Google Scholar 

  • Marin E, Nussaume L, Quesada A, Gonneau M, Sotta B, Hugueney P, Frey A and Marion-Poll A (1996) Molecular identification of zeaxanthin epoxidase of Nicotiana plumbaginifolia, a gene involved in abscisic acid biosynthesis and corresponding to the ABA locus of Arabidopsis thaliana. EMBO J 15: 2331–2342

    CAS  PubMed  Google Scholar 

  • Neubauer C and Yamamoto HY (1992) Mehler-peroxidase reaction mediates zeaxanthin formation and zeaxanthin-related fluorescence quenching in intact chloroplasts. Plant Physiol 99:1354–1361

    CAS  Google Scholar 

  • Newman T, de Bruijn FJ, Green P, Keegstra K, Kende H, McIntosh L, Ohlrogge J, Raikhel N, Somerville S, Thomashow M, Retzel E and Somerville C (1994) Genes galore: A summary of methods for accessing results from large-scale partial sequencing of anonymous Arabidopsis cDNA clones. Plant Physiol 106: 1241–1255

    Article  CAS  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Noctor G, Rees D, Young A and Horton P (1991) The relationship between zeaxanthin, energy-dependent quenching of chlorophyll fluorescence, and trans-thylakoid pH gradient in isolated chloroplasts. Biochim Biophys Acta 1057:320–330

    CAS  Google Scholar 

  • Parry AD and Horgan R (1991) Carotenoids and abscisic acid (ABA) biosynthesis in higher plants. Physiol Plant 82: 320–326

    Article  CAS  Google Scholar 

  • Pervaiz S and Brew K (1987) Homology and structure-function correlations between α1-acid glycoprotein and serum retinol-binding protein and its relatives. FASEB J 1: 209–214

    CAS  PubMed  Google Scholar 

  • Pfündel E and Strasser RJ (1988) Violaxanthin de-epoxidase in etiolated leaves. Photosynth Res 15: 67–73

    Article  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-Bennig 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 

  • Rockholm DC and Yamamoto HY (1993) Purification of violaxanthin de-epoxidase by lipid affinity precipitation. In: Yamamoto HY and Smith CM (eds) Photosynthetic Responses to the Environment, p 237. American Society of Plant Physiologists, Rockville

    Google Scholar 

  • Rockholm DC and Yamamoto HY (1996) Violaxanthin de-epoxidase: Purification of a 43-kilodalton lumenal protein from lettuce by lipid-affinity precipitation with monogalactosyl diacyl glyceride. Plant Physiol 110: 697–703

    Article  CAS  PubMed  Google Scholar 

  • Rogers S, Wells R and Rechsteiner M (1986) Amino acid sequences common to rapidly degraded proteins: The PEST hypothes is. Science 234: 364–368

    CAS  PubMed  Google Scholar 

  • Ruban AV, Young A and Horton P (1994) Modulation of chlorophyll fluorescence quenching in isolated light harvesting complex of Photosystem II. Biochim Biophys Acta 1186: 123–127

    CAS  Google Scholar 

  • Sakakibara J, Watanabe R, Kanai Y and Ono T (1995) Molecular cloning and expression of rat squalene epoxidase. J Biol Chem 270:17–20

    CAS  PubMed  Google Scholar 

  • Sapozhnikov DI, Krasovskaya TA and Maevskaya AN (1957) Change in the interrelationship of the basic carotenoids of the plastids of green leaves under the action of light. Dokl Akad Nauk 113:465–467

    CAS  Google Scholar 

  • Siefermann D (1971) Kinetic studies on the xanthophyll cycle of Lenma gibba L.—influence of photosynthetic oxygen and supplied reductor. In: Forti G, Avron M and Melandri A (eds) Proceedings IInd International Congress on Photosynthesis Research, pp 629–635. Dr. W Junk N.V. Publishers, The Hague

    Google Scholar 

  • Siefermann D and Yamamoto HY (1974) Light-induced de-epoxidation of violaxanthin in lettuce chloroplasts. III. Reaction kinetics and effect of light intensity on de-epoxidase activity and substrate availability. Biochim Biophys Acta 357: 144–150

    CAS  PubMed  Google Scholar 

  • Siefermann D and Yamamoto HY (1975a) Properties of NADPH and oxygen-dependent zeaxanthin epoxidation in isolated chloroplasts. Arch Biochem Biophys 171: 70–77

    Article  CAS  PubMed  Google Scholar 

  • Siefermann D and Yamamoto HY (1975b) Light-induced de-epoxidation of violaxanthin in lettuce chloroplasts. IV. The effects of electron-transport conditions on violaxanthin availability. Biochim Biophys Acta 387:149–158

    CAS  PubMed  Google Scholar 

  • Srivastava A and Zeiger E (1995) The inhibitor of zeaxanthin formation, dithiothreitol, inhibits blue-light-stimulated stomatal opening in Vicia faba. Planta 196: 445–449

    Article  CAS  Google Scholar 

  • Takeguchi CA and Yamamoto HY (1968) Light-induced uptake 18O2 by epoxy xanthophylls in New Zealand spinach leaves (Tetragonia expansa). Biochim Biophys Acta 153: 459–465

    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 

  • Thayer SS and Björkman O (1990) Leaf xanthophyll content and composition in sun and shade determined by HPLC. Photosynth Res 23: 331–343

    Article  CAS  Google Scholar 

  • Verhoeven AS, Demmig-Adams B and Adams WW III (1997) Enhanced employment of the xanthophyll cycle and thermal energy dissipation in spinach exposed to high light and N stress. Plant Physiol 113: 817–824

    CAS  PubMed  Google Scholar 

  • Williams WP, Gounaris K and Quinn PJ (1984) Lipid-protein interactions in the thylakoid membranes of higher plant chloroplasts. Adv Photosyn Res 3: 123–130

    CAS  Google Scholar 

  • Yamamoto HY and Higashi RM (1978) Violaxanthin de-epoxidase. Lipid composition and substrate specificity. Arch Biochem Biophys 190: 514–522

    Article  CAS  PubMed  Google Scholar 

  • Yamamoto HY, Kamite L and Wang YY (1971) An ascorbate-induced absorbance change in chloroplasts from violaxanthin de-epoxidation. Plant Physiol 49: 224–228

    Google Scholar 

  • Yamamoto H Y and Kamite L (1972) The effects of dithiothreitol on violaxanthin de-epoxidation and absorbance changes in the 500 nm region. Biochim Biophys Acta 267: 538–543

    CAS  PubMed  Google Scholar 

  • Yamamoto HY, Nakayama TOM and Chichester CO (1962) Studies on the light and dark interconversions of leaf xanthophylls. Arch Biochem Biophys 97: 168–173

    Article  CAS  PubMed  Google Scholar 

  • Young AJ, Phillip D, Ruban AV, Horton P and Frank HA (1997) The xanthophyll cycle and carotenoid-mediated dissipation of excess excitation energy in photosynthesis. Pure Appl Chem 69:2125–2130

    CAS  Google Scholar 

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© 1999 Kluwer Academic Publishers

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Yamamoto, H.Y., Bugos, R.C., David Hieber, A. (1999). Biochemistry and Molecular Biology of the Xanthophyll Cycle. 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_16

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