Abstract
Chondrus crispus (Stackhouse) is a perennial red seaweed, common in intertidal and shallow sublittoral communities throughout the North Atlantic Ocean. In the intertidal zone, C. crispus may experience rapid temperature changes of 10 to 20C° during a single immerison-emerision cycle, and may be exposed to temperatures that exceed the thermal limits for long-term survival. C. crispus collected year-round at Long Cove Point, Chamberlain, Maine, USA, during 1989 and 1990, underwent phenotypic acclimation to growth temperature in the laboratory. This phenotypic acclimation enhanced its ability to withstand brief exposure to extreme temperature. Plants grown at summer seawater temperature (20°C) were able to maintain constant rates of lightsaturated photosynthesis at 30°C for 9 h. In contrast, light-saturated photosynthetic rates of plants grown at winter seawater temperature (5°C) declined rapidly following exposure to 30°C, reached 20 to 25% of initial values within 10 min, and then remained constant at this level for 9 h. The degree of inhibition of photosynthesis at 30°C was also dependent upon light intensity. Inhibition was greatest in plants exposed to 30°C in darkness or high light (600 μmol photons m-2s-1) than in plants maintained under moderate light levels (70 to 100 μmol photons m-2s-1). Photosynthesis of 20°C-acclimated plants was inhibited by exposure to 30°C in darkness or high light, but the degree of inhibition was less than that exhibited by 5°C-grown plants. Not only was light-saturated photosynthesis of 20°C plants less severely inhibited by exposure to 30°C than that of 5°C plants, but the former also recovered faster when they were returned to growth conditions. The mechanistic basis of this acclimation to growth temperature is not clear. Our results indicate that there were no differences between 5 and 20°C-grown plants in the thermal stability of respiration, electron transport associated with Photosystems I or II, Rubisco or energy transfer between the phycobilisomes and Photosystem II. Overall, our results suggest that phenotypic acclimation to seawater temperature allows plants to tolerate higher temperatures, and may play an important role in the success of C. crispus in the intertidal environment.
Article PDF
Similar content being viewed by others
Explore related subjects
Discover the latest articles, news and stories from top researchers in related subjects.Avoid common mistakes on your manuscript.
Literature cited
Apollonio, S. (1979). The Gulf, of Maine. Courier of Maine Books, Rockland, Maine, USA
Bidwell, R. G., McLachlan, J. (1985). Carbon nutrition of seaweeds: photosynthesis; photorespiration and respiration. J. exp. mar. Biol. Ecol 86: 15–46
Bradley, P. M. (1991). Plant hormones do have a role in controlling growth and development of algae. J. Phycol. 27: 317–321
Brawley, S. H., Johnson, L. (1991). Survival of fucoid embryos in the intertidal zone depends on developmental stage and microhabitat. J. Phycol. 27: 179–186
Brinkhuis, B. H., Tempel, N. R., Jones, R. F. (1976). Photosynthesis and respiration of exposed salt-marsh fucoids. Mar. Biol. 34: 349–359
Canaani, O., Schuster, G., Ohad, I. (1989) Photoinhibition in Chlamydomonas reinhardtii: effect on state transition, intersystem energy distribution and photosystem I cyclic electron flow. Photosynthesis Res. 20: 129–146
Chapin, F. S., III, (1991). Integrated responses of plants to stress. BioSci. 41: 29–36
Chetti, M. B., Nobel, P. S. (1987). High-temperature sensitivity and its acclimation for photosynthetic electron transport reactions of desert succulents. Pl. Physiol. 84: 1063–1067
Davison, I. R. (1987) Adaptation of photosynthesis in Laminaria saccharina (Phaeophyta) to changes inggrowth temperature. J. Phycol. 23: 273–283
Davison, I. R., Dudgeon, S. R., Rhuan, H.-M. (1989) The effect of freezing on seaweed photosythesis. Mar. Ecol. Prog. Ser. 58: 123–131
Davison, I. R., Greene, R. M., Podolak, E. J. (1991). Temperature acclimation of respiration and photosynthesis in the brown alga Laminaria saccharina. Mar. Biol. 110: 449–454
Dudgeon, S. R., Davison, I. R., Vadas, R. L. (1989). Effects of freezing on photosynthesis in intertidal macroalgae: relative tolerance of Chondrus cripus and Mastocarpus stellatus (Rhodophyta). Mar. Biol. 101: 107–114
Dudgeon, S. R., Davison, I. R., Vadas, R. L. (1990). Freezing tolerance in the intertidal red algae Chondrus crispus and Mastocarpus stellatus: relative importance of acclimation and adaptation. Mar. Biol. 106: 427–436
Evans, G. C. (1972). The quantitative analysis of plant growth. Blackwell Publishing Co., Oxford
Fortes, M. D., Lüning, K. (1980). Growth rates of North Sea macroalgae in relation to temperature, irradiance, and photoperiod. Helgoländer Meeresunters. 34: 15–29
Garbary, D. J., DeWreede, R. E. (1988). Life history phases in natural populations of Gigartinaceae (Rhodophyta): quantification using resorcinol. In: Lobban, C. S., Chapman, D. J., Kremer, B. P. (eds.) Experimental phycology: a laboratory manual; Cambridge University Press, Cambridge, England.
Geider, R. J. (1987). Light and temperature dependence of the carbon to chlorophyll-a ratio in microalgae and cyanobacteria: implications for physiology and growth of phytophankton. New Phytol. 106: 1–34
Havaux, M., Greppin, H., Strasser, R. J. (1991). Functioning of photosystems I and II in pea leaves exposed to heat stress in the presence or absence of light: analysis using in-vivo fluorescence, absorbance, oxygen and photoacoustic measurements. Planta 186: 88–98
Heldt, H. W., Werdan, K., Milovancev, M., Geller, G (1983). Alkalinization of the chloroplast stroma caused by light-dependent proton flux into the thylakoid space. Biochim. biophys. Acta 314: 224–241
Kee, S. C., Nobel, P. S. (1986). Concomitant changes in high temperature tolerance and heat-shock proteins in desert succulents. Pl. Physiol. 80: 596–598
Kübler, J. E. (1992). Temperature and red algal photosynthesis. PhD. thesis. University of Maine, Orono
Kübler, J. E., Davison, I. R. (1993). Thermal acclimation of photosynthesis in the red alga, Chondrus cripus. (In preparation)
Kuebler, J. E., Davison, I. R., Yarish, C. (1991). Photosynthetic adaptation to temperature in the red algae Lomentaria baileyana and Lomentaria orcadensis. Br. phycol. J 26: 9–19
Kyle, D. J., Osmond, C. B., Arntzen, C. J. (eds.) (1987). Photoinhibition. Elsevier, Amsterdam
Lein, S. (1978). Hill reaction and photophosphorylation with chloroplast preparations from Chlamydomonas reinhardii. In: Hellebust, Craigie, J. (ed.). Handbook of phycological methods. University Press, Cambridge, p. 305–315
Lüning, K. (1984). Temperature tolerance and biogeography of seaweeds: the marine algal flora of Helgoland (North Sea) as an example. Helgoländer Meeresunters. 38: 305–317
Lüning, K. (1990). Seaweeds: their environment, biogeography and ecophysiology. Wiley & Sons, New York
Lüning, K. (1992). Day and night kinetics of growth rate in green brown and red seaweeds. J. Phycol. 28: 794–803
Mitchell, R.A.C., Barber, J. (1986). Adaptation of photosynthetic electron-transport rate to growth temperature in peas. Planta 169: 429–436
Nordhorn, G., Weidner, M., Wilenbrink, J. (1976). Isolation and photosynthetic activities of chloroplasts of the brown alga, Fucus serratus L. Z. PflPhysiol. 80: 153–165
Osmond, C. B., Austin, M. P., Berry, J. A., Billings, W. D., Boyer, J: S., Dacey, J. W. H., Nobel, P. S., Smith, S. D., Winner, W. E. (1987). Stress physiology and the distribution of plants. BioSci. 37: 38–48
Pearson, G. A., Davison, I. R. (1993). Freezing rate and duration determine the physiological response of intertidal fucoids to freezing Mar. Biol. 115: 353–362
Popovic R, Colbow, K., Vidaver, W., Bruce, D. (1983). Evolution of O2 in brown algal chloroplasts. Pl. Physiol. 73: 889–892
Powles, S.B. (1984). Photoinhibition of photosynthesis induced by visible light. A. Rev. Pl. Physiol. 35: 15–44
Provasoli, L. (1968). Media and prospects for the cultivation of marine algae. In: Watanabe, A., Hattori, A. (eds.) Cultures and collection of algae. Japanese Society of Plant Physiology, Hokane
Raven, J. A., Geider, R. J. (1988). Temperature and algal growth. New Phytol. 110: 441–461
Smith, C. M., Berry, J. A. (1986). Recovery of photosynthesis after exposure of intertidal algae to osmotic and temperature stresses: comparative studies of species with differing distribution limits. Oecologia 70: 6–12
Sommerville, C. Browse, J. (1991). Plant lipids: metabolism, mutants, and membranes. Science, N.Y. 252: 80–87
Strömgren, T. (1982). Temperature-length growth strategies in the littoral alga Ascophyllum nodosum (L.) Limnol. Oceanogr. 28: 516–521
Veirling, E. (1991). The roles of heat shock proteins in plants. A. Rev. Pl. Physiol. (Pl. molec. Biol.). 42: 579–620
Weis, E. (1982). Influence of light on the heat sensitivity of the photosynthetic apparatus in isolated spinach chloroplasts. Pl. Physiol. 70: 1530–1534
Zimmerman, R. C., Smith, R. D., Alberte, R.S. (1989). Thermal acclimation and whole plant carbon balance in Zostera marina L. (eelgrass). J. exp. mar. Biol. Ecol. 130: 93–109
Author information
Authors and Affiliations
Additional information
Communicated by J. Mauchline, Oban
Rights and permissions
About this article
Cite this article
Kübler, J.E., Davison, I.R. High-temperature tolerance of photosynthesis in the red alga Chondrus crispus . Marine Biology 117, 327–335 (1993). https://doi.org/10.1007/BF00345678
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00345678