Register      Login
Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

Diel and seasonal changes in fluorescence rise kinetics of three scleractinian corals

Ross Hill A and Peter J. Ralph A B
+ Author Affiliations
- Author Affiliations

A Institute for Water and Environmental Resource Management and Department of Environmental Sciences, University of Technology, Sydney, Westbourne Street, Gore Hill, NSW 2065, Australia.

B Corresponding author. Email: Peter.Ralph@uts.edu.au

Functional Plant Biology 32(6) 549-559 https://doi.org/10.1071/FP05017
Submitted: 21 January 2005  Accepted: 15 March 2005   Published: 15 June 2005

Abstract

The effect of diel oscillations in light on the photosynthetic response of three coral species during summer and winter was studied. Fast induction curves revealed detailed information on primary photochemistry as well as redox states of electron acceptors in photosystem II (PSII). The comparison between seasons revealed that similar physiological mechanisms were operating in response to high-light conditions throughout the year and that environmental variables, such as temperature, had no measurable effect between seasons. A diurnal hysteresis was seen in both seasons in Fv / Fm as well as in the fast induction curves, where photosynthetic capacity was lower in the afternoon than in the morning when light intensities were the same. This suggests the operation of dynamic down regulation, following exposure to midday high light. Fast induction curve analysis revealed a decline in the O, J, I and P steps towards midday and a rapid recovery by the late afternoon. The decrease in J and its rapid recovery indicated a drop in the rate of QA reduction as a result of an increase in non-photochemical quenching (NPQ). The P step increased in amplitude in the first hours of sunlight, which suggests an increased oxidation of the plastoquinone (PQ) pool and a greater capacity for electron transport. Similarly, a rise in Fv / Fm was observed within the first hour of sunlight. This response was attributed to the dark reduction of the PQ pool, induced by night time anaerobic conditions and possibly oxygen-dependent chlororespiration, which would lead to a state 2 transition. The early morning removal of chlororespiration and hypoxic conditions would have returned the photosystems to state 1, resulting in the increased photochemical efficiency of the zooxanthellae.

Keywords: chlorophyll a fluorescence, coral bleaching, diurnal hysteresis, down regulation, non-photochemical quenching, OJIP, photosystem II.


Acknowledgments

We thank N Ralph for construction of the dark-adaptation chambers, C Macinnis-Ng for advice on statistical analyses and AWD Larkum for use of the PEA fluorometer, as well as editorial comments. This work was performed with the permission of GBRMPA (permit number G01 / 623) and the Queensland EPA (permit number WITK01520603). The Australian Research Council and the University of Technology, Sydney provided funding support for PJR. Institute for Water and Environmental Resource Management contribution number 206.


References


Ambarsari I, Brown BE, Barlow RG, Britton G, Cummings D (1997) Fluctuations in algae chlorophyll and carotenoid pigments during solar bleaching in the coral Goniastrea aspera at Phuket, Thailand. Marine Ecology Progress Series 159, 303–307. open url image1

Baker, NR ,  and  Horton, P (1987). Chlorophyll fluorescence quenching during photoinhibition. In ‘Photoinhibition’. pp. 145–168. (Elsiver Science Publishers: Amsterdam)

Bennoun P (1982) Evidence for a respiratory chain in the chloroplast. Proceedings of the National Academy of Sciences USA 79, 4352–4356. open url image1

Brown BE, Le Tissier MDA, Dunne RP (1994) Tissue retraction in the scleractinian coral Coeloseris mayeri, its effect upon coral pigmentation, and preliminary implications for heat balance. Marine Ecology Progress Series 105, 209–218. open url image1

Brown BE, Ambarsari I, Warner ME, Fitt WK, Dunne RP, Gibb SW, Cummings DG (1999) Diurnal changes in photochemical efficiency and xanthophyll concentrations in shallow water reef corals: evidence for photoinhibition and photoprotection. Coral Reefs 18, 99–105.
Crossref | GoogleScholarGoogle Scholar | open url image1

Brown BE, Downs CA, Dunne RP, Gibb SW (2002) Preliminary evidence for tissue retraction as a factor in photoprotection of corals incapable of xanthophyll cycling. Journal of Experimental Marine Biology and Ecology 277, 129–144.
Crossref | GoogleScholarGoogle Scholar | open url image1

Büchel C, Wilhelm C (1990) Wavelength independent state transitions and light regulated chlororespiration as mechanisms to control the energy status in the chloroplast of Pleurochloris meiringensis. Plant Physiology and Biochemistry 28, 307–314. open url image1

Canaani O, Barber J, Malkin S (1984) Evidence that phosphorylation and dephosphorylation regulate the distribution of excitation energy between the two photosystems of photosynthesis in vivo: photoacoustic and fluorimetric study of an intact leaf. Proceedings of the National Academy of Sciences USA 81, 1614–1618. open url image1

Demmig-Adams B, Winter K (1988) Characterisation of three components of non-photochemical fluorescence quenching and their response to photoinhibition. Australian Journal of Plant Physiology 15, 163–177. open url image1

Demmig-Adams B, Adams WWI (1992) Photoprotection and other responses of plants to high light stress. Annual Review of Plant Physiology 43, 599–626.
Crossref | GoogleScholarGoogle Scholar | open url image1

Demmig-Adams, B ,  and  Adams, WWI (1993). The xanthophyll cycle. In ‘Carotenoids in photosynthesis’. pp. 206–252. (Chapman and Hall: London)

Demmig-Adams B, Winter K, Krüger A, Czygan F (1989) Light response of CO2 assimilation, dissipation of excess excitation energy, and zeaxanthin content of sun and shade leaves. Plant Physiology 90, 881–886. open url image1

Dijkman NA, Kroon BMA (2002) Indications for chlororespiration in relation to light regime in the marine diatom Thalassiosira weissflogii. Journal of Photochemistry and Photobiology. B, Biology 66, 179–187.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Garab G, Lajko F, Mustardy L, Marton L (1989) Respiratory control over photosynthetic electron transport electron in chloroplasts of higher-plant cells: evidence of chlororespiration. Planta 179, 349–358.
Crossref | GoogleScholarGoogle Scholar | open url image1

Gorbunov MY, Kolber ZS, Lesser MP, Falkowski PG (2001) Photosynthesis and photoprotection in symbiotic corals. Limnology and Oceanography 46, 75–85. open url image1

Govindjee (1995) Sixty-three years since Kautsky: chlorophyll a fluorescence. Australian Journal of Plant Physiology 22, 131–160. open url image1

Guissé B, Srivastava A, Strasser RJ (1995) The polyphasic rise of the chlorophyll a fluorescence (O-K-J-I-P) in heat stressed leaves. Archives des Sciences (Geneva) 48, 147–160. open url image1

Hill R, Larkum AWD, Frankart C, Kühl M, Ralph PJ (2004a) Loss of functional photosystem II reaction centres in zooxanthellae of corals exposed to bleaching conditions: using fluorescence rise kinetics. Photosynthesis Research 82, 59–72.
Crossref | GoogleScholarGoogle Scholar | open url image1

Hill R, Schreiber U, Gademann R, Larkum AWD, Kühl M, Ralph PJ (2004b) Spatial heterogeneity of photosynthesis and the effect of temperature-induced bleaching conditions in three species of corals. Marine Biology 144, 633–640.
Crossref | GoogleScholarGoogle Scholar | open url image1

Hill R, Frankart C, Ralph PJ (2005) Impact of bleaching conditions on the components of non-photochemical quenching in the zooxanthellae of a coral. Journal of Experimental Marine Biology and Ecology In press , open url image1

Hoegh-Guldberg O, Jones RJ (1999) Photoinhibition and photoprotection in symbiotic dinoflagellates from reef building corals. Marine Ecology Progress Series 183, 73–86. open url image1

Horton P, Hague A (1988) Studies on the induction of chlorophyll fluorescence in isolated barley protoplasts. IV. Resolution of non-photochemical quenching. Biochimica et Biophysica Acta 932, 107–115. open url image1

Horton, P ,  and  Ruban, A (1994). The role of light-harvesting complex II in energy quenching. In ‘Photoinhibition of photosynthesis: from molecular mechanisms to the field’. pp. 111–128. (BIOS Scientific Publishers: Oxford)

Jones RJ, Hoegh-Guldberg O (2001) Diurnal changes in the photochemical efficiency of the symbiotic dinoflagellates (Dionphyceae) of corals: photoprotection, photoinactivation and the relationship to coral bleaching. Plant, Cell & Environment 24, 89–99.
Crossref | GoogleScholarGoogle Scholar | open url image1

Jones RJ, Ward S, Yang AA, Hoegh-Guldberg O (2000) Changes in quantum efficiency of photosystem II of symbiotic dinoflagellates of corals after heat stress, and of bleached corals sampled after the 1998 Great Barrier Reef mass bleaching event. Marine and Freshwater Research 50, 839–866. open url image1

Kaftan D, Meszaros T, Whitmarsh J, Nedbal L (1999) Characterization of photosystem II activity and heterogeneity during the cell cycle of the green alga Scenedesmus quadricauda. Plant Physiology 120, 433–441.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Kühl M, Cohen Y, Dalsgaard T, Barker JB, Revsbech NP (1995) Microenvironment and photosynthesis of zooxanthellae in scleractinian corals studies with microsensors for O2, pH and light. Marine Ecology Progress Series 117, 159–172. open url image1

Larkum, AWD (2003). Light-harvesting systems in algae. In ‘Photosynthesis in algae’. pp. 277–304. (Kluwer Academic Publishers: The Netherlands)

Lavorel, J ,  and  Etienne, A-L (1977). In vivo chlorophyll fluorescence. In ‘Primary processes of photosynthesis’. pp. 203–268. (Elsevier: Amsterdam)

Lazár D (2003) Chlorophyll a fluorescence rise induced by high light illumination of dark-adapted plant tissue studied by means of a model of photosystem II and considering photosystem II heterogeneity. Journal of Theoretical Biology 220, 469–503.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Levy O, Dubinsky Z, Schneider K, Achituv Y, Zakai D, Gorbunov MY (2004) Diurnal hysteresis in coral photosynthesis. Marine Ecology Progress Series 268, 105–117. open url image1

Lu C, Lu Q, Zhang J, Zhang Q, Kuang T (2001) Xanthophyll cycle, light energy dissipation and photosystem II down-regulation in senescent leaves of wheat plants grown in the field. Australian Journal of Plant Physiology 28, 1023–1030. open url image1

Müller P, Li X, Niyogi KK (2001) Non-photochemical quenching. A response to excess light energy. Plant Physiology 125, 1558–1566.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Ralph PJ, Gademann R, Larkum AWD, Schreiber U (1999) In situ underwater measurements of photosynthetic activity of coral zooxanthellae and other reef-dwelling dinoflagellate endosymbionts. Marine Ecology Progress Series 180, 139–147. open url image1

Srivastava A, Guissé B, Greppin H, Strasser RJ (1997) Regulation of antenna structure and electron transport in PSII of Pisum sativum under elevated temperature probed by the fast polyphasic chlorophyll a fluorescence transient: OKJIP. Biochimica et Biophysica Acta 1320, 95–106. open url image1

Strasser, RJ ,  and  Govindjee, (1992). On the O-J-I-P fluorescence transient in leaves and D1 mutants of Chlamydomonas reinhardtii. In ‘Research in photosynthesis’. pp. 29–32. (Kluwer Academic: Dordrecht)

Strasser RJ, Srivastava A, Govindjee (1995) Polyphasic chlorophyll a fluorescence transient in plants and cyanobacteria. Photochemistry and Photobiology 61, 32–42. open url image1

Strasser RJ, Tsimilli-Michael M, Pecheux M (1999) Perpetual adaptation in a perpetually changing environment as a survival strategy of plants: a case study in forminifers concerning coral reef bleaching. Photosynthetica 37, 71–85.
Crossref | GoogleScholarGoogle Scholar | open url image1

Strasser, RJ , Tsimilli-Michael, M ,  and  Srivastava, A (2004). Analysis of the chlorophyll a fluorescence transient. In ‘Chlorophyll fluorescence: a signature of photosynthesis’. pp. 321–362. (Kluwer Academic Publishers: The Netherlands)

Thiele A, Krause GH (1994) Xanthophyll cycle and thermal energy dissipation in photosystem II: relationship between zeaxanthin and formation, energy-dependent fluorescence quenching and photoinhibition. Journal of Plant Physiology 144, 324–332. open url image1

Tsimilli-Michael, M ,  and  Strasser, RJ (2001). Fingerprints of climate change on the photosynthetic apparatus, behaviour, monitored by the JIP-test. In ‘Fingerprints of climate change’. pp. 229–247. (Kluwer Academic: New York)

Tsimilli-Michael M, Pêcheux M, Strasser RJ (1999) Light and heat stress adaptation of the symbionts of temperate and coral reef Foraminifers probed in hospite by the chlorophyll a fluorescence kinetics. Verlag der Zeitschrift für Naturforschung 54, 671–680. open url image1

Ulstrup KE, Hill R, Ralph PJ (2005) Photosynthetic impact of hypoxia on in hospite zooxanthellae in the scleractinian coral Pocillopora damicornis. Marine Ecology Progress Series 286, 125–132. open url image1

Warner ME, Fitt WK, Schmidt GW (1996) The effects of elevated temperature on the photosynthetic efficiency of zooxanthellae in hospite from four different species of coral reef: a novel approach. Plant, Cell & Environment 19, 291–299. open url image1

Warner ME, Chilcoat GC, McFarland FK, Fitt WK (2002) Seasonal fluctuations in the photosynthetic capacity of photosystem II in symbiotic dinoflagellates in the Caribbean reef-building coral Montastrea. Marine Biology 141, 31–38.
Crossref | GoogleScholarGoogle Scholar | open url image1

Winters G, Loya Y, Rottgers R, Beer S (2003) Photoinhibition in shallow-water colonies of the coral Stylophora pistillata as measured in situ. Limnology and Oceanography 48, 1388–1393. open url image1