Abstract
The violaxanthin (V)–antheraxanthin (A)–zeaxanthin (Z) (VAZ) cycle was deemed a non-second-scale process of photoprotection in higher plants and microalgae, but the validity of this view has not been confirmed. To test this view, we explored responses of the VAZ cycle and the relationship between the VAZ cycle and non-photochemical quenching (NPQ) under highlight at second and minute scales in Heterosigma akashiwo and Platymonas sp. Both A and Z were generated in H. akashiwo during 15 s of light exposure, whereas only A rapidly accumulated within 15 s of exposure in Platymonas sp. The above results, together with a time-dependent sigmoidal relationship between the VAZ cycle (de-epoxidation state, A/Chl a, and Z/Chl a) and NPQ, proved that the VAZ cycle was a second-scale process related to NPQ. In addition, we found that not all NPQ was dependent on the VAZ cycle and suggested that NPQ model should be carefully modified due to the species-specific proportions of de-epoxidation-dependent NPQ.
Similar content being viewed by others
References
Adams WW III, Demmig-Adams B, Logan BA, Barker DH, Osmond CB (1999) Rapid changes in xanthophyll cycle-dependent energy dissipation and photosystem II efficiency in two vines, Stephania japonica and Smilax australis, growing in the understory of an open Eucalyptus forest. Plant Cell Environ 22:125–136. https://doi.org/10.1046/j.1365-3040.1999.00369.x
Bidigare RR, Buttler FR, Christensen SJ, Barone B, Karl DM, Wilson ST (2014) Evaluation of the utility of xanthophyll cycle pigment dynamics for assessing upper ocean mixing processes at Station ALOHA. J Plankton Res 36:1423–1433. https://doi.org/10.1093/plankt/fbu069
Blommaert L, Huysman MJJ, Vyverman W, Lavaud J, Sabbe K (2017) Contrasting NPQ dynamics and xanthophyll cycling in a motile and a non-motile intertidal benthic diatom. Limnol Oceanogr 62:1466–1479. https://doi.org/10.1002/lno.10511
Butrón A, Madariaga I, Orive E (2012) Tolerance to high irradiance levels as a determinant of the bloom-forming Heterosigma akashiwo success in estuarine waters in summer. Estuar Coast Shelf Sci 107:141–149. https://doi.org/10.1016/j.ecss.2012.05.008
Christa G, Cruz S, Jahns P, de Vries J, Cartaxana P, Esteves AC, Serôdio J, Gould S (2017) Photoprotection in a monophyletic branch of chlorophyte algae is independent of energy-dependent quenching (qE). New Phytol 214:1132–1144. https://doi.org/10.1111/nph.14435
Demmig-Adams B, Winter K, Krüger A, Czygan F-C (1989) Zeaxanthin and the induction and relaxation kinetics of the dissipation of excess excitation energy in leaves in 2% O2, 0% CO2. Plant Physiol 90:887–893. https://doi.org/10.1104/pp.90.3.887
Demmig-Adams B, Cohu CM, Muller O, Adams WW (2012) Modulation of photosynthetic energy conversion efficiency in nature: from seconds to seasons. Photosynth Res 113:75–88. https://doi.org/10.1007/s11120-012-9761-6
Dimier C, Giovanni S, Ferdinando T, Brunet C (2009) Comparative ecophysiology of the xanthophyll cycle in six marine phytoplanktonic species. Protist 160:397–411. https://doi.org/10.1016/j.protis.2009.03.001
Ferris JM, Christian R (1991) Aquatic primary production in relation to microalgal responses to changing light: a review. Aquat Sci 53:187–217. https://doi.org/10.1007/BF00877059
Erickson E, Wakao S, Niyogi KK (2015) Light stress and photoprotection in Chlamydomonas reinhardtii. Plant J 82:449–465. https://doi.org/10.1111/tpj.12825
Falkowski PG (1983) Light-shade adaptation and vertical mixing of marine phytoplankton: a comparative field study. J Mar Res 41:215–237. https://doi.org/10.1357/002224083788520199
Frommolt R, Goss R, Wilhelm C (2001) The de-epoxidase and epoxidase reactions of Mantoniella squamata (Prasinophyceae) exhibit different substrate-specific reaction kinetics compared to spinach. Planta 213:446–456. https://doi.org/10.1007/s004250100589
Gao C, Fu M, Song H, Wang L, Wei Q, Sun P, Liu L, Zhang X (2018) Phytoplankton pigment pattern in the subsurface chlorophyll maximum in the South Java coastal upwelling system, Indonesia. Acta Oceanol Sin 37:97–106. https://doi.org/10.1007/s13131-018-1342-x
Goss R, Jakob T (2010) Regulation and function of xanthophyll cycle-dependent photoprotection in algae. Photosynth Res 106:103–122. https://doi.org/10.1007/s11120-010-9536-x
Goss R, Lepetit B (2015) Biodiversity of NPQ. J Plant Physiol 172:13–32. https://doi.org/10.1016/j.jplph.2014.03.004
Goss R, Böhme K, Wilhelm C (1998) The xanthophyll cycle of Mantoniella squamata converts violaxanthin into antheraxanthin but not to zeaxanthin: consequences for the mechanism of enhanced non-photochemical energy dissipation. Planta 205:613–621. https://doi.org/10.1007/s004250050364
Goss R, Pinto EA, Wilhelm C, Richter M (2006) The importance of a highly active and ΔpH-regulated diatoxanthin epoxidase for the regulation of the PS II antenna function in diadinoxanthin cycle containing algae. J Plant Physiol 163:1008–1021. https://doi.org/10.1016/j.jplph.2005.09.008
Guillard RR (1975) Culture of phytoplankton for feeding marine invertebrates. In: Smith WL, Chanley MH (eds) Culture of marine invertebrate animals. Springer, New York, pp 29–60
GuiryMD in GuiryMD, Guiry GM (2020) AlgaeBase. World-wide electronic publication, National University of Ireland, Galway. https://www.algaebase.org. Accessed 17 Feb 2020
Hager A (1980) The reversible, light-induced conversions of xanthophylls in the chloroplast. In: Czygan F-C (ed) Pigments in plants. Fischer, Stuttgart, pp 57–79
Hennige S, Coyne KJ, Macintyre HL, Liefer JD, Warner ME (2013) The photobiology of Heterosigma akashiwo. Photoacclimation, diurnal periodicity, and its ability to rapidly exploit exposure to high light. J Phycol 49:349–360. https://doi.org/10.1111/jpy.12043
Holzwarth AR, Miloslavina Y, Nilkens M, Jahns P (2009) Identification of two quenching sites active in the regulation of photosynthetic light-harvesting studied by time-resolved fluorescence. Chem Phys Lett 483:262–267. https://doi.org/10.1016/j.cplett.2009.10.085
Jahns P, Holzwarth AR (2012) The role of the xanthophyll cycle and of lutein in photoprotection of photosystem II. Biochim Biophys Acta 1817:182–193. https://doi.org/10.1016/j.bbabio.2011.04.012
Johnson MP, Davison PA, Ruban AV, Horton P (2008) The xanthophyll cycle pool size controls the kinetics of non-photochemical quenching in Arabidopsis thaliana. FEBS Lett 582:262–266. https://doi.org/10.1016/j.febslet.2007.12.016
Lohr M, Wilhelm C (1999) Algae displaying the diadinoxanthin cycle also possess the violaxanthin cycle. Proc Natl Acad Sci USA 96:8784–8789. https://doi.org/10.1073/pnas.96.15.8784
Macintyre HL, Kana TM, Geider RJ (2000) The effect of water motion on short-term rates of photosynthesis by marine phytoplankton. Trends Plant Sci 5:12–17. https://doi.org/10.1016/S1360-1385(99)01504-6
Maxwell K, Johnson GN (2000) Chlorophyll fluorescence—a practical guide. J Exp Bot 51:659–668. https://doi.org/10.1093/jexbot/51.345.659
Müller P, Li X, Niyogi KK (2001) Non-photochemical quenching. A response to excess light energy. Plant Physiol 125:1558–1566. https://doi.org/10.1104/pp.125.4.1558
Nilkens M, Kress E, Lambrev PH, Miloslavina Y, Muller M, Holzwarth AR, Jahns P (2010) Identification of a slowly inducible zeaxanthin-dependent component of non-photochemical quenching of chlorophyll fluorescence generated under steady-state conditions in Arabidopsis. Biochim Biophys Acta 1797:466–475. https://doi.org/10.1016/j.bbabio.2010.01.001
Olaizola M, Kolber ZS, Falkowski PG (1994) Non-photochemical fluorescence quenching and the diadinoxanthin cycle in a marine diatom. Photosynth Res 41:357–370. https://doi.org/10.1007/BF00019413
Olaizola M, Yamamoto HY (1994) Short-term response of the diadinoxanthin cycle and fluorescence yield to high irradiance in Chaetoceros muelleri (Bacillariophyceae). J Phycol 30:606–612. https://doi.org/10.1111/j.0022-3646.1994.00606.x
Quaas T, Berteotti S, Ballottari M, Flieger K, Bassi R, Wilhelm C, Goss R (2015) Non-photochemical quenching and xanthophyll cycle activities in six green algal species suggest mechanistic differences in the process of excess energy dissipation. J Plant Physiol 172:92–103. https://doi.org/10.1016/j.jplph.2014.07.023
Rodríguez F, Chauton MS, Johnsen G, Andresen K, Olsen LM, Zapata M (2006) Photoacclimation in phytoplankton: implications for biomass estimates, pigment functionality and chemotaxonomy. Mar Biol 148:963–971. https://doi.org/10.1007/s00227-005-0138-7
Schubert H, Sagert S, Forster RM (2001) Evaluation of the different levels of variability in the underwater light field of a shallow estuary. Helgol Mar Res 55:12–22. https://doi.org/10.1007/s101520000064
Tian L, Nawrocki WJ, Liu X, Polukhina I, Van Stokkum IHM, Croce R (2019) PH dependence, kinetics and light-harvesting regulation of nonphotochemical quenching in Chlamydomonas. Proc Natl Acad Sci USA 116:8320–8325. https://doi.org/10.1073/pnas.1817796116
Wobbe L, Bassi R, Kruse O (2016) Multi-level light capture control in plants and green Algae. Trends Plant Sci 21:55–68. https://doi.org/10.1016/j.tplants.2015.10.004
Yamamoto HY (1979) Biochemistry of the violaxanthin cycle in higher plants. Pure Appl Chem 51:639–648. https://doi.org/10.1016/B978-0-08-022359-9.50017-5
Yamamoto HY, 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. https://doi.org/10.1016/0005-2728(72)90182-X
Acknowledgements
We thank editor and two anonymous reviewers for their constructive and helpful advice on the manuscript. We thank Prof. Yan Zhao at the Ocean University of China for her kind comments on the original manuscript. This work was supported by the National Key Research and Development Program of China (2016YFC1402100), the NSFC-Shandong Joint Funded Project “Marine Ecology and Environmental Sciences” (U1606404) and the foundation of the China Ocean Mineral Resources R & D Association (DY135-E2-4).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Sun, KM., Gao, C., Zhang, J. et al. Rapid formation of antheraxanthin and zeaxanthin in seconds in microalgae and its relation to non-photochemical quenching. Photosynth Res 144, 317–326 (2020). https://doi.org/10.1007/s11120-020-00739-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11120-020-00739-6