The Xanthophyll Cycle in Green Algae (Chlorophyta): Its Role in the Photosynthetic Apparatus

Abstract

Light-dependent conversion of violaxanthin to zeaxanthin, the so-called xanthophyll cycle, was shown to serve as a major, short-term light acclimation mechanism in higher plants. The role of xanthophylls in thermal dissipation of surplus excitation energy was deduced from the linear relationship between zeaxanthin formation and the magnitude of non-photochemical quenching. Unlike in higher plants, the role of the xanthophyll cycle in green algae (Chlorophyta) is ambiguous, since its contribution to energy dissipation can significantly vary among species. Here, we have studied the role of the xanthophyll cycle in the adaptation of several species of green algae (Chlorella, Scenedesmus, Haematococcus, Chlorococcum, Spongiochloris) to high irradiance. The xanthophyll cycle has been found functional in all tested organisms; however its contribution to non-photochemical quenching is not as significant as in higher plants. This conclusion is supported by three facts: (i) in green algae the content of zeaxanthin normalized per chlorophyll was significantly lower than that reported from higher plants, (ii) antheraxanthin + zeaxanthin content displayed different diel kinetics from NPQ and (iii) in green algae there was no such linear relationship between NPQ and Ax + Zx, as found in higher plants. We assume that microalgae rely on other dissipation mechanism(s), which operate along with xanthophyll cycle-dependent quenching.

Key words

Microalgae - fluorescence - non-photochemical quenching - photobioreactor - zeaxanthin - violaxanthin

References

• 1 Adams W. W., Demmig-Adams B., Verhoeven A. S., Barker D. H.. “Photoinhibition” during winter stress: involvement of sustained xanthophyll-cycle-dependent energy dissipation.  Australian Journal of Plant Physiology. (1995);  22 261-276
• 2 Bocci F., Torzillo G., Vincenzini M., Materassi R.. Growth physiology of Spirulina platensis in tubular photobioreactor under sunlight. Stadler, T., Mollion, J., Verdus, M. C., Karamanos, Y., Morvan, H., and Christiaen, D., eds. Algal Biotechnology. London; Elsevier Applied Sciences Publishers (1987): 219-228
• 3 Boussiba S., Lu F., Vonshak A.. Astaxanthin accumulation in the green alga Haematococcus pluvialis. .  Plant Cell Physiology. (1991);  32 1077-1082
• 4 Casper-Lindley C., Björkman O.. Fluorescence quenching in four unicellular algae with different light-harvesting and xanthophyll-cycle pigments.  Photosynthesis Research. (1998);  56 277-289
• 5 Demmig B., Winter K., Krüger A., Czygan F.-C.. Photoinhibition and zeaxanthin formation in intact leaves.  Plant Physiology. (1987);  84 218-224
• 6 Demmig-Adams B.. Carotenoids and photoprotection in plants. A role for the xanthophyll zeaxanthin.  Biochimica et Biophysica Acta. (1990);  1020 1-24
• 7 Demmig-Adams B., Adams W. W.. Xanthophyll cycle and light stress in nature: uniform response to excess direct sunlight among higher plant species.  Planta. (1996);  198 460-470
• 8 Frank H. A., Cua A., Chynwat V., Young A., Gosztola D., Wasielewski M. R.. Photophysics of the carotenoids with the xanthophyll cycle in photosynthesis.  Photosynthesis Research. (1994);  41 389-395
• 9 Gilmore A. M.. Mechanistic aspects of xanthophyll cycle-dependent photoprotection in higher plant chloroplasts and leaves.  Physiologia Plantarum. (1997);  99 197-209
• 10 Gilmore A. M., Yamamoto H. Y.. Zeaxanthin formation and energy dependent fluorescence quenching in pea chloroplasts under artificially mediated linear and cyclic electron transport.  Plant Physiology. (1991);  96 635-643
• 11 Gilmore A. M., Yamamoto H. Y.. Linear models relating xanthophylls and lumen acidity to non-photochemical fluorescence quenching. Evidence that antheraxanthin explains zeaxanthin-independent quenching.  Photosynthesis Research. (1993);  35 67-78
• 12 Hager A.. Lichtbedingte pH-Erniedrigung in einem Chloroplasten-Kompartiment als Ursache der enzymatischen Violaxanthin-Zeaxanthin-Umwandlung; Beziehungen zur Photophosphorylierung.  Planta. (1969);  89 224-243
• 13 Hager A., Holocher K.. Localization of the xanthophyll-cycle enzyme violaxanthin de-epoxidase with the thylakoid lumen and abolition of its mobility by a (light-dependent) pH decrease.  Planta. (1994);  192 581-589
• 14 Horton P., Ruban A. V., Walters R. G.. Regulation of light harvesting in green plants.  Annual Reviews of Plant Physiology and Plant Molecular Biology. (1996);  47 655-684
• 15 Horton P., Ruban A. V., Rees D., Pascal A. A., Noctor G., Young A. J.. Control of the light-harvesting function of chloroplast membranes by aggregation of the LHCII chlorophyll-protein function.  FEBS Letters. (1991);  292 1-4
• 16 Ivanov A. G., Sane P., Hurry V., Krol M., Sveshnikov D., Huner N. P. A., Oquist G.. Low-temperature modulation of the redox properties of the acceptor side of photosystem II: photoprotection through reaction centre quenching of excess energy.  Physiologia Plantarum. (2003);  119 376-383
• 17 Jin E. S., Yokthongwattana K., Polle J. E. W., Melis A.. Role of the reversible xanthophylls cycle in the Photosystem II damage and repair cycle in Dunaliella salina. .  Plant Physiology. (2003);  132 352-364
• 18 Koblížek M., Ciscato M., Komenda J., Kopecký J., Šiffel P., Masojídek J.. Light adaptation in Spongiochloris sp. A three-fluorometer study.  Photosynthetica. (1999);  37 307-323
• 19 Krause G. H.. Photoinhibition of photosynthesis. An evaluation of damaging and protecting mechanisms.  Physiologia Plantarum. (1988);  74 566-574
• 20 Li X.-P., Björkman O., Shih C., Grossman A. R., Rosenquist M., Jansson S., Niyogi K. K.. A pigment-binding protein essential for regulation of photosynthetic light harvesting.  Nature. (2000);  403 391-395
• 21 Lichtenthaler H. K., Schindler C.. Studies on the photoprotective function of zeaxanthin at high-light conditions. Murata, N., ed. Research in Photosynthesis, Vol. IV. Dordrecht; Kluwer Academic Publishers (1992): 517-520
• 22 Lichtenthaler H. K., Wellburn A. R.. Determination of total carotenoids and chlorophyll a and b of leaf extracts in different solvents.  Biochemical Society Transactions. (1983);  603 591-592
• 23 Lichtenthaler H. K., Burkart S., Schindler C., Stober F.. Changes in photosynthetic pigments and in vivo chlorophyll fluorescence parameters under photoinhibitory growth conditions.  Photosynthetica. (1992);  27 343-353
• 43 Ma Y.-Z., Holt N. E., Li X.-P., Niyogi K. K., Fleming G. R.. Evidence for direct carotenoid involvement in the regulation of photosynthetic light harvesting.  Proceedings of the National Academy of Sciences of the USA. (2003);  100 4377-4382
• 24 Masojídek J., Papáček Š., Sergejevová M., Jirka V., Červený J., Kunc J., Korečko J., Verbovikova O., Kopecký J., Štys D., Torzillo G.. A closed solar photobioreactor for cultivation of microalgae under supra-high irradiance: basic design and performance.  Journal of Applied Phycology. (2003);  15 239-248
• 25 Masojídek J., Torzillo G., Koblížek M., Kopecký J., Bernardini P., Sacchi A., Komenda J.. Photoadaptation of two members of the Chlorophyta (Scenedesmus and Chlorella) in laboratory and outdoor cultures: changes of chlorophyll fluorescence quenching and the xanthophyll cycle.  Planta. (1999);  209 126-135
• 26 Masojídek J., Torzillo G., Kopecky J., Koblížek M., Nidiaci L., Komenda J., Lukavská A., Sacchi A.. Changes in chlorophyll fluorescence quenching and pigment composition in the green alga Chlorococcum sp. grown under nitrogen deficiency and salinity stress.  Journal of Applied Phycology. (2000);  12 417-426
• 27 Nedbal L., Koblížek M.. Chlorophyll fluorescence as a reporter on in vivo electron transport and regulation in plants. Grimm, B., Porra, R., Rüdiger, W., and Scheer, H., eds. Biochemistry and Biophysics of Chlorophylls. Dordrecht; Kluwer Academic Press (2004)
• 28 Neubauer C.. Multiple effects of dithiothreitol on non-photochemical fluorescence quenching in intact chloroplasts.  Plant Physiology. (1993);  103 575-583
• 29 Niyogi K., Björkman O., Grossman A. R.. Chlamydomonas xanthophyll cycle mutants identified by video imaging of chlorophyll fluorescence quenching.  Plant Cell. (1997 a);  9 1369-1380
• 30 Niyogi K., Björkman O., Grossman A. R.. The roles of specific xanthophylls in photoprotection.  Proceedings of the National Academy of Sciences of the USA. (1997 b);  94 14162-14167
• 31 Olaizola M.. Commercial production of astaxanthin from Haematococcus pluvialis using 25 000-liter outdoor photobioreactors.  Journal of Applied Phycology. (2000);  12 499-506
• 32 Pfündel E., Bilger W.. Regulation and possible function of the violaxanthin cycle.  Photosynthesis Research. (1994);  42 89-109
• 33 Polívka T., Herek J. L., Zigmantas D., Akerlund H. E., Sundström V.. Direct observation of the (forbidden) S1 state in carotenoids.  Proceedings of the National Academy of Sciences of the USA. (1999);  96 4914-4917
• 34 Rise M., Cohen E., Vishkautsan M., Cojocaru M., Gottlieb H. E., Arad S.. Accumulation of secondary carotenoids in Chlorella zofingiensis. .  Journal of Plant Physiology. (1994);  44 287-292
• 35 Ruban A. V., Phillip D., Young A. J., Horton P.. Carotenoid-dependent oligomerization of the major chlorophyll a/b light-harvesting complex of photosystem II of plants.  Biochemistry. (1997);  36 7855-7859
• 36 Sapozhnikov D. I., Krasovskaya T. A., Maevskaya A. N.. Change in the interrelationship of the basic carotenoids of the green leaves under the action of light.  Doklady Akademii Nauk USSR. (1957);  113 465-467
• 37 Schindler C., Lichtenthaler H. K.. Is there a correlation between light-induced zeaxanthin accumulation and quenching of variable chlorophyll a fluorescence?.  Plant Physiology and Biochemistry. (1994);  32 813-823
• 38 Schindler C., Lichtenthaler H. K.. Photosynthetic CO₂-assimilation, chlorophyll fluorescence and zeaxanthin accumulation in field grown maple trees in the course of a sunny and a cloudy day.  Journal of Plant Physiology. (1996);  148 399-412
• 39 Seaton G. G. R., Hurry V. M., Rohozinski J.. Novel amplification of non-photochemical chlorophyll fluorescence quenching following viral infection in Chlorella. .  FEBS Letters. (1996);  389 319-323
• 40 Torzillo G., Goksan T., Faraloni C., Kopecky J., Masojidek J.. Interplay between photochemical activities and pigment composition in an outdoor culture of Haematococcus pluvialis during the shift from the green to red stage.  Journal of Applied Phycology. (2003);  15 127-136
• 41 Yamamoto H., Nakayama O. M., Chichester C. O.. Studies on the light and dark interconversions of leaf xanthophylls.  Archives of Biochemistry and Biophysics. (1962);  97 168-173
• 42 Zhang D. H., Lee Y. K., Ng M. L., Phang S. M.. Composition and accumulation of secondary carotenoids in Chlorococcum sp.  Journal of Applied Phycology. (1997);  9 147-155

Guest Editor: F. Loreto