Plant Biol (Stuttg) 2003; 5(4): 366-377
DOI: 10.1055/s-2003-42716
Original Paper

Georg Thieme Verlag Stuttgart · New York

The Effect of Elevated UV Radiation on Fucus spp. (Fucales, Phaeophyta) Zygote and Embryo Development

M. E. A. Schoenwaelder 1 , C. Wiencke 1 , M. N. Clayton 2 , K. W. Glombitza 3
  • 1Foundation Alfred Wegener Institute for Polar and Marine Research, Bremerhaven, Germany
  • 2School of Biological Sciences, Monash University, Victoria, Australia
  • 3Institute for Pharmaceutical Biology, Bonn, Germany
Further Information

Publication History

Publication Date:
02 October 2003 (online)

Abstract

This study has shown that in Fucus serratus and Fucus distichus, young zygotes and embryos are highly susceptible to elevated levels of both UVA (UVAR) and UVB radiation (UVBR). Zygotes treated with UVAR are able to polarise and germinate, but are very slow to divide; if they do, they often have skewed division planes or deformed rhizoids. Those treated with UVAR and UVBR remain spherical, they do not polarise, germinate to form rhizoids or undergo cell division. We suggest that the UVR may be affecting the cytoskeleton. Conversely, zygotes and embryos of Fucus spiralis are able to withstand these same UVR levels and, at the light microscope level, appear to develop normally. When the brown algal phenolic compound phloroglucinol was placed in a filter covering the developing embryos, normal development was seen under all treatments. Phenolic compounds protect the developing fucoids from UVR. In comparison with the other two species, Fucus spiralis grows high up on the shore and is exposed for much longer periods of time and, presumably, to higher levels of natural UVR. The failure of the juvenile stages of F. serratus and F. distichus to withstand UVR stress may have implications for the continued survival of these species in the intertidal, and may prove detrimental to the population as a whole if UVR levels increase.

References

  • 1 Allen D. J., Nogués S., Baker N. R.. Ozone depletion and increased UV-B radiation: is there a real threat to photosynthesis?.  Journal of Experimental Botany. (1998);  49 1775-1788
  • 2 Allen V. W., Kropf D. L.. Nuclear rotation and lineage specification in Pelvetia embryos.  Development. (1992);  115 873-883
  • 3 Antonelli F., Bussotti D., Grifoni P., Grossoni B., Mori B., Tani C., Zipoli G.. Oak (Quercus robur L.) seedlings responses to a realistic increase in UV-B radiation under open space conditions.  Chemosphere. (1998);  36 841-845
  • 4 Bachereau F., Marigo G., Asta J.. Effect of solar radiation (UV and visible) at high altitude on CAM-cycling and phenolic compound biosynthesis in Sedum album. .  Physiologia Plantarum. (1998);  104 203-210
  • 5 Barnes P. W., Jordan P. W., Gold W. G., Flint S. D., Caldwell M. M.. Competition, morphology and canopy structure in wheat (Triticum aestivum L.) and wild oat (Avena fatua L.) exposed to enhanced ultra-violet-B radiation.  Functional Ecology. (1988);  2 319-330
  • 6 Bass E. L., Sistrum S. N.. Effect of UVA radiation on development and hatching success in Oryzias latipes, the Japanese medaka.  Bulletin of Environmental Contamination Toxicology. (1997);  59 537-542
  • 7 Basu S., Sun H., Brian L., Quatrano R. L., Muday G. K.. Early embryo development in Fucus distichus is auxin sensitive.  Plant Physiology. (2002);  130 292-302
  • 8 Berthold G.. Beiträge zur Morphologie und Physiologie der Meeresalgen.  Jahrbuch für Wissenschaftliche Botanik. (1882);  13 569-717
  • 9 Biebl R.. Lichtresistenz von Meeresalgen.  Protoplasma. (1956);  46 63-89
  • 10 Bischof K., Hanelt D., Wiencke C.. Acclimation of maximal quantum yield of photosynthesis in the brown alga Alaria esculenta under high light and UV radiation.  Plant Biology. (1999);  1 435-444
  • 11 Bisgrove S. R., Kropf D. L.. Cell wall deposition during morphogenesis in fucoid algae.  Planta. (2001);  212 648-658
  • 12 Blaustein A. R., Hoffman P. D., Hokit D. G., Kiesecker J. M., Walls S. C., Hays J. B.. UV repair and resistance to solar UV-B in amphibian eggs: a link to population declines?.  Proceedings of the National Academy of Sciences USA. (1994);  91 1791-1795
  • 13 Blumthaler M., Ambach W.. Indication of increasing solar ultraviolet-B radiation flux in alpine regions.  Science, NY. (1990);  248 206-208
  • 14 Bothwell M. L., Sherbot D., Roberge A. C., Daley R. J.. Influence of natural ultraviolet radiation on lotic periphytic diatom community growth, biomass accrual, and species composition: short-term versus long-term effects.  Journal of Phycology. (1994);  29 24-35
  • 15 Brawley S. H., Johnson L. E.. Survival of fucoid embryos in the intertidal zone depends upon developmental stage and microhabitat.  Journal of Phycology. (1991);  27 179-186
  • 16 Brawley S. H., Quatrano R.. Sulfation of fucoidin in Fucus embryos. IV. Autoradiographic investigations of fucoidin sulfation and secretion during differentiation and the effect of cytochalasin treatment.  Developmental Biology. (1979);  73 193-205
  • 17 Brawley S. H., Robinson K. R.. Cytochalasin treatment disrupts the endogenous currents associated with cell polarization in fucoid zygotes: studies of the role of F-actin in embryogenesis.  Journal of Cell Biology. (1985);  100 1173-1184
  • 18 Bussotti F., Gravano E., Grossoni P., Tano C.. Occurrence of tannins in leaves of beech trees (Fagus sylvatica) along an ecological gradient, detected by histochemical and ultrastructural analyses.  New Phytologist. (1998);  138 469-479
  • 19 Caasi-Lit M., Whitecross M. I., Nayudu M., Tanner G. J.. UV-B Irradiation induces differential leaf damage, ultrastructural changes and accumulation of specific phenolic compounds in rice cultivars.  Australian Journal of Plant Physiology. (1997);  24 261-274
  • 20 Caldwell M. M., Robberrecht R., Flint S. D.. Internal filters: prospects for UV-acclimation in higher plants.  Physiologica Plantarum. (1983);  58 445-450
  • 21 Caldwell M. M., Björn L. O., Bornman J. F., Flint S. D., Kulandaivelu G., Teramura A. H., Tevini M.. Effects of increased solar ultraviolet radiation on terrestrial ecosystems.  Journal of Photochemistry and Photobiology B: Biology. (1998);  46 40-52
  • 22 Chapman A. R. O.. Functional ecology of fucoid algae: twenty-three years of progress.  Phycologia. (1995);  34 1-32
  • 23 Cockell C. S., Knowland J.. Ultraviolet radiation screening compounds.  Biological Review. (1999);  74 311-345
  • 24 Coelho S. M., Rijstenbil J. W., Brown M. T.. Impacts of anthropogenic stresses on the early development stages of seaweeds.  Journal of Aquatic Ecosystem Stress and Recovery. (2000);  7 317-333
  • 25 Cooper-Driver G. A., Bhattacharya M.. Role of phenolics in plant evolution.  Phytochemistry. (1998);  49 1165-1174
  • 26 Cordi B., Donkin M. E., Peloquin J., Price D. N., Depledge M. H.. The influence of UV-B radiation on the reproductive cells of the intertidal macroalga, Enteromorpha intestinalis. .  Aquatic Toxicology. (2001);  56 1-11
  • 27 Cronin G., Hay M. E.. Susceptibility to herbivores depends on recent history of both the plant and animal.  Ecology. (1996);  77 1531-1543
  • 28 Cullen J. J., Neale P. J., Lesser M. P.. Biological weighting function for the inhibition of phytoplankton photosynthesis by ultraviolet radiation.  Science. (1992);  258 646-650
  • 29 Davison I., Johnson L. E., Brawley S. H.. Sublethal stress in the intertidal zone: tidal emersion inhibits photosynthesis and retards development in embryos of the brown alga Pelvetia fastigiata. .  Oecologia. (1993);  96 483-492
  • 30 Dring M. J., Makarov V., Schoschina E., Lorenz M., Lüning K.. Influence of ultraviolet-radiation on the chlorophyll fluorescence and growth in different life-history stages of three species of Laminaria (Phaeophyta).  Marine Biology. (1996);  126 183-191
  • 31 Duarte C. M.. Submerged aquatic vegetation in relation to different nutrient regimes.  Ophelia. (1995);  41 87-112
  • 32 Dunton K. H., Schell D. M.. Dependence of consumers on macroalgal (Laminaria solidungula) carbon in an arctic community: δ13C evidence.  Marine Biology. (1987);  93 615-625
  • 33 Dunton K. H.. Del 15 N and del 13 C measurements of Antarctic peninsula fauna: trophic relationships and assimilation of benthic seaweeds.  American Zoologist. (2001);  41 99-112
  • 34 Epel D., Hemela K., Shick M., Patton C.. Development in the floating world: defenses of eggs and embryos against damage from UV radiation.  American Zoologist. (1999);  39 271-278
  • 35 Flint S. D., Jordan P. W., Caldwell M. M.. Plant protective response to enhanced UV-B radiation under field conditions: leaf optical properties and photosynthesis.  Photochemistry and Photobiology. (1985);  41 95-99
  • 36 Franklin L. A., Forster R. M.. The changing irradiance environment: consequences for marine macrophyte physiology productivity and ecology.  European Journal of Phycology. (1997);  32 207-232
  • 37 Ganesan M., Mairh O. P., Eswaran K., Subba Rao P. V.. Effect of UV radiation and other environmental factors on the liberation of tetraspores from brown alga Padina boergesenii (Phaeophyta, Dictyotales).  Indian Journal of Marine Sciences. (1999);  28 50-54
  • 38 Grant P., Wacaster J. F.. The amphibian grey crescent - a site of developmental information?.  Developmental Biology. (1972);  28 454-471
  • 39 Han T., Kain (Jones) J. M.. Effect of photon irradiance and photoperiod on young sporophytes of four species of the Laminariales.  European Journal of Phycology. (1996);  31 233-240
  • 40 Hanelt D., Wiencke C., Nultsch W.. Influence of UV radiation on the photosynthesis of Arctic macroalgae in the field.  Journal of Photochemistry and Photobiology B: Biology. (1997 a);  38 40-47
  • 41 Hanelt D., Wiencke C., Karsten U., Nultsch W.. Photoinhibition and recovery after high light stress in different developmental and life history stages of Laminara saccharina (Phaeophyta).  Journal of Phycology. (1997 b);  33 38-395
  • 42 Jeffery W. R.. An ultraviolet-sensitive maternal mRNA encoding a cytoskeletal protein may be involved in axis formation in the Ascidian embryo.  Developmental Biology. (1990);  141 141-148
  • 43 Kaur I., Vijayaraghavan M. R.. Physode distribution and genesis in Sargassum vulgare C. Agardh and Sargassum johnstonii Setchell & Gardner.  Aquatic Botany. (1992);  42 375-384
  • 44 Kerr J. B., McElroy C. T.. Evidence for large upward trends of ultraviolet-B radiation linked to ozone depletion.  Science, NY. (1993);  262 1032-1034
  • 45 Kevekordes K.. The effects of secondary-treated effluent and reduced salinity on specific events in the early life stages of Hormosira banksii (Phaeophyceae).  European Journal of Phycology. (2000);  35 365-371
  • 46 Kornmann P., Sahling P. H.. Meeresalgen von Helgoland. Benthische Grün-, Braun- und Rotalgen. Hamburg; Biologische Anstalt Helgoland (1977): 162-172
  • 47 Kouwenberg J. H. M., Browman H. I., Runge J. A., Cullen J. J., Davis R. F., St-Pierre J. F.. Biological weighting of ultraviolet (280 - 400 nm) induced mortality in marine zooplankton and fish. II. Calanus finmarchicus eggs.  Marine Biology. (1999);  134 285-293
  • 48 Kropf D. L.. Role of the cytoskeleton in cellular morphogenesis of zygotes of fucoid algae. Menzel, D., ed. The Cytoskeleton of the Algae. CRC Press (1992): 79-92
  • 49 Kropf D. L.. Cytoskeletal control of cell polarity in a plant zygote.  Developmental Biology. (1994);  165 361-371
  • 50 Kropf D. L.. Induction of polarity in fucoid zygotes.  The Plant Cell. (1997);  9 1011-1020
  • 51 Kropf D. L.. Microtubule disruption and function in early Pelvetia development.  Journal of Cell Science. (1990);  97 545-552
  • 52 Kropf D. L., Money N. P., Gibbon B. C.. Role of cytosolic pH in axis establishment and tip growth.  Canadian Journal of Botany. (1995);  73 S126-S130
  • 53 Kropf D. L., Bisgrove S. R., Hable W. E.. Establishing a growth axis in fucoid algae.  Trends in Plant Sciences. (1999);  4 490-494
  • 54 Lüning K.. Critical levels of light and temperature regulating the gametogenesis of three Laminaria species (Phaeophyceae).  Journal of Phycology. (1980);  16 1-15
  • 55 Lüning K., Neushul M.. Light and temperature demands for growth and reproduction of Laminaria gametophytes in Southern and Central California.  Marine Biology. (1978);  45 297-309
  • 56 Makarov M. V., Voskoboinikov G. M.. The influence of UVR on spore release and growth of the kelp Laminaria saccharina. .  Botanica Marina. (2001);  44 89-94
  • 57 Malm T., Kautsky L., Engkvist R.. Reproduction, recruitment and geographic distribution of Fucus serratus L. in the Baltic sea.  Botanica Marina. (2001);  44 101-108
  • 58 McLachlan J., Craigie J. S.. Algal inhibition by yellow ultraviolet-absorbing substances from Fucus vesiculosus. .  Canadian Journal of Botany. (1964);  42 287-292
  • 59 Mohle B., Wellmann E.. Induction of phenylpropanoid compounds by UV-B irradiation in roots of seedlings and cell cultures from Dill (Anethum gaveolens L.).  Plant Cell Reports. (1982);  1 183-185
  • 60 Motomura T.. Electron and immunofluorescence microscopy on the fertilization of Fucus distichus. .  Protoplasma. (1994);  178 97-110
  • 61 Nelson D. R., Jaffe L. F.. Cells without cytoplasmic movements respond to cytochalasin.  Developmental Biology. (1973);  30 206-208
  • 62 Pavia H., Cervin G., Lindgren A., Åberg P.. Effects of UV-B radiation and simulated herbivory on phlorotannins in the brown alga Ascophyllum nodosum. .  Marine Ecology Progress Series. (1997);  157 139-146
  • 63 Pearson G. A., Brawley S. H.. Reproductive ecology of Fucus distichus (Phaeophyceae): an intertidal alga with successful external fertilization.  Marine Ecology Progress Series. (1996);  143 211-223
  • 64 Pontillon C.. Sur les variations quantitatives du fucosane dans le Fucus serratus L.  Compte Rendu de l'Académie des Sciences. (1926);  95 970-971
  • 65 Quatrano R. S.. Separation processes associated with differentiation of two-celled Fucus embryos.  Developmental Biology. (1973);  30 209-213
  • 66 Rafferty N. S., Rafferty K. A., Zigman S.. Comparitive response to UV irradiation of cytoskeletal elements in rabbit and skate lens epithelial cells.  Current Eye Research. (1997);  16 310-319
  • 67 Ragan M. A.. Physodes and the phenolic compounds of brown algae. Composition and significance of physodes in vivo. .  Botanica Marina. (1976);  XIX 145-154
  • 68 Ragan M. A., Glombitza K. W.. Phlorotannins, brown algal polyphenols. Round, F. E. and Chapman, D. J., eds. Progress in Phycological Research 4. Bristol; Biopress Ltd. (1986): 129-241
  • 69 Rex M., Harris N. R. P., Gathen P., von der Lehmann R., Braathen G. O., Reimer E., Beck A., Chipperfield M. P., Alfier R., Allaart M., O'Connor F., Dier H., Dorokhov V., Fast H., Gil M., Kyrö E., Litynska Z., Mikkelsen I. S., Molyneux M. G., Nakane H., Notholt J., Rummukainen M., Viatte P., Wenger J.. Prolonged stratospheric ozone loss in the 1995/96 Arctic winter.  Nature. (1997);  389 835-838
  • 70 Rijstenbil J. W., Coelho S. M., Eijsackers M.. A method for the assessment of light induced oxidative stress in embryos of fucoid algae via confocal laserscan microscopy.  Marine Biology. (2000);  137 763-774
  • 71 Robinson K. R., Wozniak M., Pu R., Messerli M.. Symmetry breaking in the zygotes of the fucoid algae: controversies and recent progress.  Current Topics in Developmental Biology. (1999);  44 101-125
  • 72 Rodriguez C. A., Browman H. I., Runge J. A., St-Pierre J. F.. Impact of solar UV radiation on hatching of a marine copeopod, Calanus finmarchicus. .  Marine Ecology Progress Series. (2000);  193 85-93
  • 73 Rozema J., van de Staaij J., Björn L. O., Caldwell M.. UV-B as an environmental factor in plant life: stress and regulation.  Trends in Ecology and Evolution. (1997);  12 22-28
  • 74 Scharf E. R., Gerhart J. C.. Axis determination in eggs of Xenopus laevis: a critical period before first cleavage, identified by the common effects of cold, pressure and ultraviolet irradiation.  Developmental Biology. (1983);  99 75-87
  • 75 Schnitzler J. P., Jungblut T. P., Heller W., Köfferlein M., Hutzler P.,  Heinzmann U., Schmelzer E., Ernst D., Langebartels C., Sandermann  Jr. H.. Tissue localization of UV-B screening pigments and of chalcone synthase mRNA in needles of Scots pine seedlings.  New Phytologist. (1996);  32 247-258
  • 76 Schoenwaelder M. E. A.. The occurrence and cellular significance of physodes in brown algae. Phycological Reviews 21.  Phycologia. (2002);  41 125-139
  • 77 Schoenwaelder M. E. A., Clayton M. N.. The secretion of phenolic compounds following fertilization in Acrocarpia paniculata (Fucales, Phaeophyta).  Phycologia. (1998 a);  37 40-46
  • 78 Schoenwaelder M. E. A., Clayton M. N.. Secretion of phenolic substances into the zygote wall and cell plate in embryos of Hormosira and Acrocarpia (Fucales, Phaeophyceae).  Journal of Phycology. (1998 b);  34 969-980
  • 79 Schoenwaelder M. E. A., Clayton M. N.. The role of the cytoskeleton in brown algal physode movement.  European Journal of Phycology. (1999);  34 223-229
  • 80 Schoenwaelder M. E. A., Wiencke C.. Phenolic compounds in the embryo development of several northern hemisphere fucoids.  Plant Biology. (2000);  2 24-33
  • 81 Sinha R. P., Klisch M., Gröniger A., Häder D. P.. Ultraviolet-absorbing/screening substances in cyanobacteria, phytoplankton and macroalgae.  Journal of Photochemistry and Photobiology B: Biology. (1998);  47 83-94
  • 82 Somosy Z.. Radiation responses of cell organelles.  Micron. (2000);  31 165-181
  • 83 Stapleton A., Walbot V.. Flavonoids can protect maize DNA from the induction of ultraviolet radiation damage.  Plant Physiology. (1994);  105 881-889
  • 84 Strahle S., Jesuthasan U.. Ultraviolet irradiation impairs epiboly in zebrafish embryos: Evidence for a microtubule-dependent mechanism of epiboly.  Development. (1993);  119 909-919
  • 85 Swanson A. K., Druehl L. D.. Differential meiospore size and tolerance of ultraviolet light stress within and among kelp species along a depth gradient.  Marine Biology. (2000);  136 657-664
  • 86 Swanson A. K., Druehl L. D.. Introduction, exudation and the UV protection role of kelp phlorotannins.  Aquatic Botany. (2002);  73 241-253
  • 87 Tevini M., Braun J., Fieser G.. The protective function of the epidermal layer of rye seedlings against ultraviolet-B radiation.  Photochemistry and Photobiology. (1991);  53 329-333
  • 88 Tugwell S., Branch G. M.. Differential polyphenolic distribution among tissues in the kelps Ecklonia maxima, Laminaria pallida and Macrocystis angustifolia in relation to plant-defence theory.  Journal of Experimental Marine Biology and Ecology. (1989);  129 219-230
  • 89 Turunen M., Heller W., Stich S., Sandermann H., Sutinen M. L., Norokorpi Y.. The effects of UV exclusion on the soluble phenolics of young Scots pine seedlings in the subarctic.  Environmental Pollution. (1999);  106 219-228
  • 90 Tyrell R. M.. UVA (320 - 380 nm) radiation as an oxidative stress. Sies, H., ed. Oxidative Stress: Oxidants and Antioxidants. San Diego; Academic Press (1991): 57-83
  • 91 Wellmann E.. UV dose-dependent induction of enzymes related to flavonoid biosynthesis in cell suspension cultures of parsley.  FEBS Letters. (1975);  51 105-107
  • 92 Wiencke C., Gómez I., Pakker H., Flores-Moya A., Altamirano M., Hanelt D., Bischof K., Figueroa F. L.. Impact of UV radiation on viability, photosynthetic characteristics and DNA of brown algal zoospores: implications for depth zonation.  Marine Ecology Progress Series. (2000);  197 217-229
  • 93 Williamson C. E., Metzgar S. L., Lovera P. A., Moeller R. E.. Solar UV radiation and the spawning habit of yellow perch, Perca flavescens. .  Ecological Applicaitons. (1997);  7 1017-1023
  • 94 Wood W. F.. Effect of solar ultra-violet radiation on the kelp Ecklonia radiata. .  Marine Biology. (1987);  96 143-150
  • 95 Zamansky G. B., Nguyen U., Chou I. N.. An immunofluorescence study of the effects of ultraviolet radiation on the organization of microfilaments, keratin intermediate filaments, and microtubules in human keratinocytes.  Cell Motility and the Cyto-skeleton. (1992);  22 296-306

M. Schoenwaelder

Foundation Alfred Wegener Institute for Polar and Marine Research

Am Handelshafen 12

27570 Bremerhaven

Germany

Email: moschoenwaelder@awi-bremerhaven.demonicaeas@yahoo.co.uk

Section Editor: G. Thiel