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Thallus morphology and optical characteristics affect growth and DNA damage by UV radiation in juvenile Arctic Laminaria sporophytes

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Abstract

Growth of young sporophytes of the brown algae Laminaria digitata, L. saccharina and L. solidungula from Spitsbergen were measured in the laboratory after being exposed for 21 days to either photosynthetically active radiation (PAR=P) or to full light spectrum (PAR + UV-A + UV-B=PAB) using of cutoff glass filters. The plants were grown at 8±2°C and 16 h light : 8 h dark cycles with 6 h additional ultraviolet radiation (UVR) exposure in the middle of the light period. Growth was measured every 10 min using growth chambers with online video measuring technique. Tissue morphology and absorption spectra were measured in untreated young sporophytes while chlorophyll (Chl) a content and DNA damage were measured in treated thalli at the end of the experiment. In all species, growth rates were significantly higher in sporophytes exposed to P alone compared to sporophytes exposed to PAB. Tissue DNA damage is dependent on thallus thickness and absorption spectra characteristics of pigments and UV-absorbing compounds. In sporophytes exposed to UVR, energy demands for repair of DNA damage and synthesis of UV-absorbing compounds for protection effectively diverts photosynthate at the expense of growth. Photosynthetic pigment was not significantly different between treatments suggesting a capacity for acclimation to moderate UVR fluence. The general growth pattern in sporophytes exposed to P alone showed an increasing growth rate from the onset of light (0500–0900 hours) to a peak at the middle of the light phase (0900–1500 hours), a decline towards the end of the light phase (1500–2100 hours) and a minimum “low” growth in the dark (2100–0500 hours) relative to growth during the entire light phase. Under PAB, different growth patterns were observed such as growth compensation at night in L. digitata, delayed growth recovery in L. saccharina and minimal but continuous growth in L. solidungula. Growth as an integrative parameter of all physiological processes showed that the effect of UVR is correlated to the depth distribution of these species.

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Abbreviations

PAR:

Photosynthetically active radiation

UV-A:

Ultraviolet-A

UV-B:

Ultraviolet-B

UVR:

UV radiation

P:

PAR

PAB:

PAR + UV-A + UV-B

PFD:

Photon flux density

Chl:

Chlorophyll

References

  • Aguilera J, Karsten U, Lippert H, Vögele B, Philipp E, Hanelt D, Wiencke C (1999) Effects of solar radiation on growth, photosynthesis and respiration of marine macroalgae from the Arctic. Mar Ecol Progr Ser 191:109–119

    Article  Google Scholar 

  • Aguilera J, Bischof K, Karsten U, Hanelt D, Wiencke C (2002) Seasonal variation in ecophysiological patterns in macroalgae from an Arctic fjord. II. Pigment accumulation and biochemical defence systems against high light stress. Mar Biol 140:1087–1095

    Article  CAS  Google Scholar 

  • Altamirano M, Flores-Moya A, Figueroa F-L (2000) Long-term effects of natural sunlight under various ultraviolet radiation conditions on growth and photosynthesis of intertidal Ulva rigida (Chlorophyceae) cultivated in situ. Bot Mar 43:19–26

    Article  Google Scholar 

  • Arnold TM (2003) To grow and defend: lack of tradeoffs for brown algal phlorotannins. Oikos 100:406–408

    Article  Google Scholar 

  • Bischof K, Hanelt D, Tüg H, Karsten U, Brouwer PEM, Wiencke C (1998) Acclimation of brown algal photosynthesis to ultraviolet radiation in Arctic coastal waters (Spitsbergen, Norway). Polar Biol 20:388–395

    Article  Google Scholar 

  • Bischof K, Hanelt D, Aguilera J, Karsten U, Vögele B, Sawall T, Wiencke C (2002a) Seasonal variation in ecophysiological patterns in macroalgae from an Arctic fjord. I. Sensitivity of photosynthesis to ultraviolet radiation. Mar Biol 140:1097–1106

    Article  CAS  Google Scholar 

  • Bischof K, Kräbs G, Wiencke C, Hanelt D (2002b) Solar ultraviolet radiation affects the activity of ribulose-1,5-biphosphate carboxylase-oxygenase and the composition of photosynthetic and xanthophyll cycle pigments in the intertidal green alga Ulva lactuca L. Planta 215:502–509

    Article  CAS  Google Scholar 

  • Borum J, Pedersen MF, Krause-Jensen D, Christensen PB, Nielsen K (2002) Biomass, photosynthesis and growth of Laminaria saccharina in a high-arctic fjord, NE Greenland. Mar Biol 141:11–19

    Article  Google Scholar 

  • Brinkhuis BH (1985) Growth pattern and rates. In: Littler MM, Littler DS (eds) Handbook of phycological methods: ecological field methods: macroalgae. Cambridge University Press, Cambridge, pp 461–477

    Google Scholar 

  • Busdosh M, Beehler CL, Robilliard GA, Tarbox KR (1985) Distribution and abundance of kelp in the Alaskan Beaufort Sea near Prudhoe Bay. Arctic 38:18–22

    Google Scholar 

  • Caldwell MM (1971) Solar ultraviolet radiation and the growth and development of higher plants. In: Giese AC (ed). Photophysiology. Academic Press, New York, pp 131–177

    Google Scholar 

  • Caldwell MM, Robberecht R, Flint SD (1983) Internal filters: prospects for UV-acclimation in higher plants. Physiol Plant 58:445–450

    Article  CAS  Google Scholar 

  • Carr GM, Duthie HC, Taylor WD (1997) Models of aquatic plant productivity: a review of the factors that influence growth. Aquat Bot 59:195–215

    Article  Google Scholar 

  • Chapman ARO, Lindley JE (1980) Seasonal growth of Laminaria solidungula in the Canadian high Arctic in relation to irradiance and dissolved nutrient concentrations. Mar Biol 57:1–5

    Article  CAS  Google Scholar 

  • Dring MJ, Makarov V, Schoschina E, Lorenz M, Lüning K (1996) Influence of ultraviolet-radiation on chlorophyll fluorescence and growth in different life-history stages of three species of Laminaria (Phaeophyta). Mar Biol 126:183–191

    Article  CAS  Google Scholar 

  • Dunton KH (1985) Growth of dark-exposed Laminaria saccharina (L.) Lamour, and Laminaria solidungula J. Ag. (Laminariales: Phaeophyta) in the Alaskan Beaufort Sea. J Exp Mar Biol Ecol 94:181–189

    Article  Google Scholar 

  • Dunton KH (1990) Growth and production in Laminaria solidungula: relation to continuous underwater light levels in the Alaskan High Arctic. Mar Biol 106:297–304

    Article  Google Scholar 

  • Dunton KH, Jodwalis CM (1988) Photosynthetic performance of Laminaria solidungula measured in situ in the Alaskan High Arctic. Mar Biol 98:277–285

    Article  Google Scholar 

  • Franklin LA, Forster RM (1997) The changing irradiance environment: consequences for marine macrophyte physiology, productivity and ecology. Eur J Phycol 32: 207–232

    Google Scholar 

  • Hanelt D, Wiencke C, Nultsch W (1997) Influence of UV radiation on photosynthesis of Arctic macroalgae in the field. J Photochem Photobiol B Biol 38:40–47

    Article  CAS  Google Scholar 

  • Hanelt D, Tüg GH, Bischof K, Groß C, Lippert H, Sawall T, Wiencke C (2001) Light regime in an Arctic fjord: a study related to stratospheric ozone depletion as a basis for determination of UV effects on algal growth. Mar Biol 138:649–658

    Article  CAS  Google Scholar 

  • Henley WJ, Dunton KH (1995) A seasonal comparison of carbon, nitrogen, and pigment content in Laminaria solidungula and L. saccharina (Phaeophyta) in the Alaskan Arctic. J Phycol 31:325–331

    Article  Google Scholar 

  • Henry BE, van Alstyne KL (2004) Effects of UV radiation on growth and phlorotannins in Fucus gardneri (Phaeophyceae) juveniles and embryos. J Phycol 40:527–533

    Article  CAS  Google Scholar 

  • Hop H, Pearson T, Hegseth EN, Kovacs KM, Wiencke C, Kwasniewski S, Eiane K, Mehlum F, Gulliksen B, Wlodarska-Kowalczuk M, Lydersen C, Weslawski JM, Cochrane S, Gabrielsen GW, Leakey RJG, Lønne OJ, Zajaczkowski M, Falk-Petersen S, Kendall M, Wängberg S-Å, Bischof K, Voronkov AY, Kovaltchouk NA, Wiktor J, Poltermann M, di Prisco G, Papucci C, Gerland S (2002) The marine ecosystem of Kongsfjorden, Svalbard. Polar Res 21:167–208

    Article  Google Scholar 

  • Johansson G, Snoeijs P (2002) Macroalgal photosynthetic responses to light in relation to thallus morphology and depth zonation. Mar Ecol Prog Ser 244:63–72

    Article  Google Scholar 

  • Karsten U, Bischof K, Wiencke C (2001) Photosynthetic performance of Arctic macroalgae after transplantation from deep to shallow waters followed by exposure to natural solar radiation. Oecologia 127:11–20

    Article  Google Scholar 

  • Landry LG, Chapple CCS, Last RL (1995) Arabidopsis mutants lacking phenolic sunscreens exhibit enhanced ultraviolet-B injury and oxidative damage. Plant Physiol 109:1159–1166

    Article  PubMed  CAS  Google Scholar 

  • Long SP, Humphries S, Falkowski PG (1994) Photoinhibition of photosynthesis in nature. Ann Rev Plant Physiol Plant Mol Biol 45:633–662

    Article  CAS  Google Scholar 

  • Lüder UH, Clayton MN (2004) Induction of phlorotannins in the brown algae Ecklonia radiata (Laminariales, Phaeophyta) in response to simulated herbivory- the first microscopic study. Planta 218:928–937

    Article  PubMed  CAS  Google Scholar 

  • Lüning K (1979) Growth strategies of three Laminaria species (Phaeophyceae) inhabiting different depth zones in the sublittoral region of Helgoland (North Sea). Mar Ecol Prog Ser 1:195–207

    Article  Google Scholar 

  • Lüning K (1992) Day and night kinetics of growth rate in green, brown, and red seaweeds. J Phycol 28:794–803

    Article  Google Scholar 

  • Lüning K (1994) Circadian growth rhythm in juvenile sporophytes of Laminariales (Phaeophyta) J Phycol 30:193–199

    Article  Google Scholar 

  • Michler T, Aguilera J, Hanelt D, Bischof K, Wiencke C (2002) Long-term effects of ultraviolet radiation on growth and photosynthetic performance of polar and cold-temperate macroalgae. Mar Biol 140:1117–1127

    Article  CAS  Google Scholar 

  • van de Poll WH, Eggert A, Buma AGJ, Breeman AM (2001) Effects of UV-B induced DNA damage and photoinhibition on growth of temperate marine red macrophytes: habitat-related differences in UV-B tolerance. J Phycol 37:30–37

    Article  Google Scholar 

  • van de Poll WH, Hanelt D, Hoyer K, Buma AGJ, Breeman AM (2002) Ultraviolet-B induced cyclobutane-pyrimidine dimer formation and repair in Arctic marine macrophytes. Photochem Photobiol 76:493–501

    Article  PubMed  Google Scholar 

  • Poppe F, Hanelt D, Wiencke C (2002) Changes in ultrastructure, photosynthetic activity and pigments in the Antarctic red alga Palmaria decipiens during acclimation to UV radiation. Bot Mar 45:253–261

    Article  CAS  Google Scholar 

  • Rijstenbil JW, Coelho SM, Eijsackers M (2000) A method for the assessment of light-induced oxidative stress in embryos of fucoid algae via confocal laserscan microscopy. Mar Biol 137:763–774

    Article  CAS  Google Scholar 

  • Robberecht R, Caldwell MM (1978) Leaf epidermal transmittance of ultraviolet radiation and its implications for plant sensitivity to ultraviolet-radiation induced injury. Oecologia (Berl.) 32:277–287

    Article  Google Scholar 

  • Roleda MY, van de Poll WH, Hanelt D, Wiencke C (2004a) PAR and UVBR effects on photosynthesis, viability, growth and DNA in different life stages of two coexisting Gigartinales: implications for recruitment and zonation pattern. Mar Ecol Prog Ser 281:37–50

    Article  Google Scholar 

  • Roleda MY, Hanelt D, Kräbs G, Wiencke C (2004b) Morphology, growth, photosynthesis and pigments in Laminaria ochroleuca (Laminariales, Phaeophyta) under ultraviolet radiation. Phycologia 43:603–613

    Article  Google Scholar 

  • Roleda MY, Wiencke C, Hanelt D, van de Poll WH, Gruber A (2005a) Sensitivity of Laminariales zoospores from Helgoland (North Sea) to ultraviolet and photosynthetically active radiation: implications for depth distribution and seasonal reproduction. Plant Cell Environ 28:466–479

    Article  Google Scholar 

  • Roleda MY, Hanelt D, Wiencke C (2005b) Growth kinetics related to physiological parameters in young Saccorhiza dermatodea and Alaria esculenta sporophytes exposed to UV radiation. Polar Biol 28:539–549

    Article  Google Scholar 

  • Setlow RB (1974) The wavelengths in sunlight effective in producing skin cancer: a theoretical analysis. Proc Nat Acad Sci USA 71:3363–3366

    Article  PubMed  CAS  Google Scholar 

  • Shibata T, Kawaguchi S, Hama Y, Inagaki M, Yamaguchi K, Nakamura T (2004) Local and chemical distribution of phlorotannins in brown algae. J Appl Phycol 16:291–296

    Article  CAS  Google Scholar 

  • Stapleton AE, Walbot V (1994) Flavonoids protect maize DNA from the induction of ultraviolet radiation damage. Plant Physiol 105:881–889

    Article  PubMed  CAS  Google Scholar 

  • Starr RC, Zeikus JA (1993) UTEX—the culture collection of algae at the University of Texas at Austin. J Phycol 29 (Suppl):1–106

    Article  Google Scholar 

  • Vink AA, Bergen-Henegouwen JB, Nikaido O, Baan RP, Roza L (1994) Removal of UV-induced DNA lesions in mouse epidermis soon after irradiation. Photochem Photobiol 24:25–31

    Article  CAS  Google Scholar 

  • Wiencke C, Gómez I, Pakker H, Flores-Moya A, Altamirano M, Hanelt D, Bischof, K, Figueroa F-L (2000) Impact of UV radiation on viability, photosynthetic characteristics and DNA of brown algal zoospores: implications for depth zonation. Mar Ecol Prog Ser 197:217–229

    Article  Google Scholar 

  • Wiencke C, Clayton MN, Schoenwaelder M (2004) Sensitivity and acclimation to UV radiation of zoospores from five species of Laminariales from the Arctic. Mar Biol 145:31–39

    Article  Google Scholar 

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Acknowledgements

MY Roleda is supported by a scholarship from the German Academic Exchange Service (DAAD). We thank the diving team of Spitsbergen 2004 campaign for collecting field materials and C Daniel for pigment analysis. This is publication awi-n 15194 of the Alfred Wegener Institute for Polar and Marine Research.

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Correspondence to Michael Y. Roleda.

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Roleda, M.Y., Wiencke, C. & Hanelt, D. Thallus morphology and optical characteristics affect growth and DNA damage by UV radiation in juvenile Arctic Laminaria sporophytes. Planta 223, 407–417 (2006). https://doi.org/10.1007/s00425-005-0092-0

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