Photosynthetica 2018, 56(3):799-810 | DOI: 10.1007/s11099-017-0731-2

Comparative study of the effects of salinity and UV radiation on metabolism and morphology of the red macroalga Acanthophora spicifera (Rhodophyta, Ceramiales)

D. T. Pereira1, C. Simioni1, L. C. Ouriques1, F. Ramlov2, M. Maraschin2, N. Steiner3, F. Chow4, Z. L. Bouzon1, É. C. Schmidt1,*
1 Plant Cell Biology Laboratory, Department of Cell Biology, Embryology and Genetics, Federal University of Santa Catarina, Florianópolis, SC, Brazil
2 Plant Morphogenesis and Biochemistry Laboratory, Federal University of Santa Catarina, Florianópolis, SC, Brazil
3 Plant Physiology Laboratory, Department of Botany, Federal University of Santa Catarina, Florianópolis, SC, Brazil
4 Institute of Bioscience, University of São Paulo, São Paulo, SP, Brazil

Increase of harmful radiation to the Earth's surface due to ozone depletion results in higher exposure to harmful ultraviolet- B radiation (UV), while fluctuations in seawater salinity may alter water density, ionic concentration, nutrient uptake, and osmotic pressure. This study evaluated the effects of salinity and UV on metabolism and morphology of Acanthophora spicifera (M.Vahl) Børgesen. Water with 30 and 37 psu [g(salt) kg-1(sea water)] was used for experiments during 7 d of exposure to UV (3 h per day). We demonstrated that UV treatment predisposed, irrespective of salinity, A. spicifera to a decrease in its growth rate and cell viability, as well as affected its morphological parameters. After exposure to PAR + UVA + UVB (PAB), samples showed structural changes and damage, such as increasing cell wall thickness and chloroplast disruption. Our results indicate that UV led to dramatic metabolic changes and cellular imbalances, but more remarkable changes were seen in samples exposed to high salinity.

Keywords: alga; cell viability; growth rate; metabolites; microscopy

Received: January 12, 2017; Accepted: March 19, 2017; Prepublished online: September 1, 2018; Published: August 1, 2018Show citation

ACS AIP APA ASA Harvard Chicago IEEE ISO690 MLA NLM Turabian Vancouver
Pereira, D.T., Simioni, C., Ouriques, L.C., Ramlov, F., Maraschin, M., Steiner, N., ... Schmidt, É.C. (2018). Comparative study of the effects of salinity and UV radiation on metabolism and morphology of the red macroalga Acanthophora spicifera (Rhodophyta, Ceramiales). Photosynthetica56(3), 799-810. doi: 10.1007/s11099-017-0731-2.
Download citation

Supplementary files

Download filephs-201803-0005_S1.pdf

File size: 137.87 kB

Download filephs-201803-0005_S2.pdf

File size: 189.46 kB

References

  1. Aguilera J., Karsten U., Lippert H. et al.: Effects of solar radiation on growth, photosynthesis and respiration of marine macroalgae from the Arctic.-Mar. Ecol.-Prog. Ser. 191: 109-119, 1999. Go to original source...
  2. Aminot A., Chaussepied M.: [Manual of Chemical Analyzes in Marine Environment.] Pp. 379. CNEXO, Brest 1983. [In French]
  3. Araújo F.O., Ursi S., Plastino E.M.: Intraspecific variation in Gracilaria caudata (Gracilariales, Rhodophyta): growth, pigment content, and photosynthesis.-J. Appl. Phycol. 26: 849-858, 2014. Go to original source...
  4. Baghel R.S., Kumari P., Reddy C.R.K., Jha B.: Growth, pigments, and biochemical composition of marine red alga Gracilaria crassa.-J. Appl. Phycol. 26: 2143-2150, 2014. Go to original source...
  5. Balogh T.S., Velasco M.V.R., Pedriali C.A. et al.: [Protection against ultraviolet radiation: features currently available under photoprotection.]-Ann. Bras. Dermatol. 86: 732-42, 2011. [In Portuguese] Go to original source...
  6. Baltruschat H., Fodor J., Harrach B.D. et al.: Salt tolerance of barley induced by the root endophyte Piriformospora indica is associated with a strong increase in antioxidants.-New Phytol. 180: 501-510, 2008. Go to original source...
  7. Barros M.P., Necchi O., Colepicolo P. et al.: Kinetic study of the plastoquinone pool availability correlated with H2O2 release in seawater and antioxidant responses in the red alga Kappaphycus alvarezii exposed to single or combined high light, chilling and chemical stresses.-BBA-Bioenergetics 1757: 1520-1528, 2006. Go to original source...
  8. Bartley M.L., Boeing W.J., Corcoran A.A. et al.: Effects of salinity on growth and lipid accumulation of biofuel microalga Nannochloropsis salina and invading organisms.-Biomass Bioenerg. 54: 83-88, 2013. Go to original source...
  9. Batista R.D., Batista R.D., Santos G.R. et al.: [Antioxidative responses in cowpea nodules inoculated with bradyrhizobium.]-Desafios 2: 76-88, 2015. [In Portuguese]
  10. Berridge M.V., Herst P.M., Tan A.S.: Tetrazolium dyes as tools in cell biology: new insights into their cellular reduction.-Biotechnol. Annu. Rev. 11: 127-152, 2005. Go to original source...
  11. Biever, J.J., Brinkman D., Gardner G.: UV-B inhibition of hypocotyl growth in etiolated Arabidopsis thaliana seedlings is a consequence of cell cycle arrest initiated by photodimer accumulation.-J. Exp. Bot. 65: 2949-2961, 2014. Go to original source...
  12. Bischof K., Hanelt D., Wiencke C.: Effects of ultraviolet radiation on photosynthesis and related enzyme reactions marine macroalgae.-Planta 211: 555-562, 2000. Go to original source...
  13. Bischof K., Kräbs G., Wiencke C. et al.: Solar ultraviolet radiation affects the activity of ribulose-1, 5-bisphosphate carboxylase-oxygenase and the composition of photosynthetic and xanthophyll cycle pigments in the intertidal green alga Ulva lactuca L.-Planta 215: 502-509, 2002. Go to original source...
  14. Borderie F., Laurence A.S., Naoufal R. et al.: UV-C irradiation as a tool to eradicate algae in caves.-Int. Biodeter. Biodegr. 65: 579-584, 2011. Go to original source...
  15. Bradford M.M.: A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding.-Anal. Biochem. 72: 248-254, 1976. Go to original source...
  16. Cavalcanti F.R., Lima J.P.M., Ferreira-Silva S.L. et al.: Roots and leaves display contrasting oxidative response during salt stress and recovery in cowpea.-J. Plant Physiol. 164: 591-600, 2007. Go to original source...
  17. Choo K.S., Snoeijs P., Pedersén M.: Oxidative stress tolerance in the filamentous green algae Cladophora glomerata and Enteromorpha ahlneriana.-J. Exp. Mar. Biol. Ecol. 298: 111-123, 2004.
  18. Chow F., Macchiavello J., Cruz S.S. et al.: Utilization of Gracilaria chilensis (Rhodophyta: Gracilariaceae) as a biofilter in the depuration of effluents from tank cultures of fish, oysters, and sea urchins.-J. World Aquacult. Soc. 32: 2515-220, 2001. Go to original source...
  19. Chow F.: Nitrate assimilation: the role of in vitro nitrate reductase assay as nutritional predictor.-In: Najafpour M.M. (ed.): Applied Photosynthesis. Pp. 105-120. In Tech, Croatia 2012. Go to original source...
  20. Connan S., Stengel D.B.: Impacts of ambient salinity and copper on brown algae: 2. Interactive effects on phenolic pool and assessment of metal binding capacity of phlorotannin.-Aquat. Toxicol. 104: 1-13, 2011. Go to original source...
  21. Costa V.M.F.: [Use of the macroalgae Ulva lactuca Linnaeus in nutrient reduction (NH4+, NO3-e PO-24) from shrimp farming.]-PhD Thesis, Federal University of Rio Grande do Norte, 2006. [In Portuguese]
  22. Cronin G., Lodge D.M.: Effects of light and nutrient availability on the growth, allocation, carbon/nitrogen balance, phenolic chemistry, and resistance to herbivory of two freshwater macrophytes.-Oecologia 137: 32-41, 2003. Go to original source...
  23. Dailer M.L., Smith J.E., Smith C.E.: Responses of bloom forming and non-bloom forming macroalgae to nutriente enrichment in Hawaii, USA.-Harmful Algae 17: 111-125, 2012. Go to original source...
  24. de Almeida S.L., Schmidt E.C., Pereira D.T. et al.: Effect of ultraviolet-B radiation in laboratory on morphological and ultrastructural characteristics and physiological parameters of selected cultivar of Oryza sativa L.-Protoplasma 250: 1303-1313, 2013. Go to original source...
  25. de Azevedo Neto A.D., Prisco J.T., Enéas-Filho J. et al.: Effect of salt stress on antioxidative enzymes and lipid peroxidation in leaves and roots of salt-tolerant and salt-sensitive maize genotypes.-Environ. Exp. Bot. 56: 87-94, 2006. Go to original source...
  26. de Reviers B.: [Biology and Phylogeny of Algae. 2nd ed.] Pp. 280. Artmed, Brazil 2006. [In Portuguese]
  27. De Tullio M.C.: Antioxidants and redox regulation: Changing notions in a changing world.-Plant Physiol. Bioch. 48: 289-291, 2010. Go to original source...
  28. Devi M.P., Subhash G.V., Mohan S.V.: Heterotrophic cultivation of mixed microalgae for lipid accumulation and wastewater treatment during sequential growth and starvation phases: effect of nutrient supplementation.-Renew. Energ. 43: 276-283, 2012. Go to original source...
  29. Diffey B.L.: Sources and measurement of ultraviolet radiation.-Methods 28: 4-13, 2002. Go to original source...
  30. Duarte M.E., Cauduro J.P., Noseda D.G. et al.: The structure of the agaran sulfate from Acanthophora spicifera (Rhodomelaceae, Ceramiales) and its antiviral activity. Relation between structure and antiviral activity in agarans.-Carbohydr. Res. 339: 335-347, 2004. Go to original source...
  31. Edwards P.: Cultured red alga to measure pollution.-Mar. Pollut. Bull. 3: 184-188, 1972. Go to original source...
  32. Felix M.R., Osorio L.K., Ouriques L.C. et al.: The effect of cadmium under different salinity conditions on the cellular architecture and metabolism in the red alga Pterocladiella capillacea (Rhodophyta, Gelidiales).-Microsc. Microanal. 20: 1411-1424, 2014. Go to original source...
  33. Fialho F.A.N.: [Integrated multitrophic aquaculture: macroalgae biofilters in the culture of the arrowhead.]-Completion of course work of the Federal University of Santa Catarina, 2013. [In Portuguese]
  34. Fidantsef A.L., Britt A.B.: Preferential repair of the transcribed DNA strand in plants.-Front. Plant Sci. 2: 105, 2012.
  35. Figueroa F.L., Domínguez-González B., Korbee N.: Vulnerability and acclimation to increased UVB radiation in three intertidal macroalgae of different morpho-functional groups.-Mar. Environ. Res. 97: 30-38, 2014.
  36. Fong P., Boyer K.E., Desmond J.S., Zedler J.B.: Salinity stress, nitrogen competition, and facilitation: what controls seasonal succession of two opportunistic green macroalgae?-J. Exp. Mar. Biol. Ecol. 206: 203-221, 1996. Go to original source...
  37. Forzza R.C., Baumgratz J.F.A., Bicudo C.E.M. et al.: New Brazilian floristic list highlights conservation challenges.-BioScience 62: 39-45, 2012. Go to original source...
  38. Franceschini I. M., Burliga A. L., de Reviers B. et al.: [Algae: a phylogenetic, taxonomic and ecological approach.] Pp. 19-57. Artmed, Brazil 2010. [In Portuguese]
  39. Fukayama H., Ueguchi C., Nishikawa K. et al.: Overexpression of Rubisco activase decreases the photosynthetic CO2 assimilation rate by reducing Rubisco content in rice leaves.-Plant Cell Physiol. 53: 976-986, 2012. Go to original source...
  40. Ganesan P., Kumar C.S., Bhaskar N.: Antioxidant properties of methanol extract and its solvent fractions obtained from selected Indian red seaweeds.-Bioresour. Technol. 99: 2717-2723, 2008. Go to original source...
  41. Gill S.S., Tuteja N.: Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants.-Plant Physiol. Bioch. 48: 909-930, 2010. Go to original source...
  42. Gómez I., Huovinen P.: Morpho-functional patterns and zonation of South Chilean seaweeds: the importance of photosynthetic and bio-optical traits.-Mar. Ecol. Prog. Ser. 422: 77-91, 2011. Go to original source...
  43. Gordon E.M., McCandless E.L.: Ultrastructure and histochemistry of Chondrus crispus Stackhouse.-Nova Scotia Inst. Sci. Proc. 27: 111-133, 1973.
  44. He Y.Y., Häder D.P.: Reactive oxygen species and UV-B: effect on cyanobacteria.-Photoch. Photobio. Sci. 1: 729-736, 2002. Go to original source...
  45. Heo S.J., Ko S.C., Kang S.M. et al.: Cytoprotective effect of fucoxanthin isolated from brown algae Sargassum siliquastrum against H2O2-induced cell damage.-Eur. Food Res. Technol. 228: 145-151, 2008.
  46. Heo S.J., Ko S., Kang S. et al.: Inhibitory effect of diphlorethohydroxycarmalol on melanogenesis and its protective effect against UV-B radiation-induced cell damage.-Food Chem. Toxicol. 48: 1355-1361, 2010. Go to original source...
  47. Holzinger A., Lütz C.: Algae and UV irradiation: effects on ultrastructure and related metabolic functions.-Micron 37: 190-207, 2006. Go to original source...
  48. Horn R.A.: The effect of litopenaeus stylirostris aquaculture on macroalgae growth in opunohu Bay, moorea, French polynesia.-Stud. Res. Papers 1: 1-12, 2012.
  49. Ifeanyi V.O., Anyanwu B.N., Ogbulie J.N. et al.: Determination of the effect of light and salt concentrations on Aphanocapsa algal population.-Afr. J. Microbiol. Res. 5: 2488-2492, 2011.
  50. Jayasankar R.: Effect of salinity on physiology of Gracilaria spp. (Gigartinales, Rhodophyta).-Seaweed Res. Util. 27: 19-24, 2005.
  51. Jormalainen V., Honkanen T., Koivikko R. et al.: Induction of phlorotannin production in a brown alga: defense or resource dynamics?-Oikos 103: 640-650, 2003. Go to original source...
  52. Kalbina I., Strid A.: The role of NADPH oxidase and MAP kinase phosphatase in UV-B-dependent gene expression in Arabidopsis.-Plant Cell Environ. 29: 1783-1793, 2006. Go to original source...
  53. Lang K.L.: [Chemical and biological research of red algae Acanthophora spicifera (Vahl) Borgesen.]-PhD. Thesis of Federal University of Santa Catarina, 2006. [In Portuguese]
  54. Li X., Zhang L., Li Y. et al.: Changes in photosynthesis, antioxidant enzymes and lipid peroxidation in soybean seedlings exposed to UV-B radiation and/or Cd.-Plant Soil 352: 377-387, 2012. Go to original source...
  55. Lin C.C., Kao C.H.: Cell wall peroxidase activity, hydrogen peroxide level and NaCl-inhibited root growth of rice seedlings.-Plant Soil 230: 135-143, 2001. Go to original source...
  56. Lobban C.S., Harrison P.J.: Temperature and salinity.-In: Lobban C.S., Harrison P.J. (ed.): Seaweed Ecology and Physiology. Pp. 210-240. Cambridge Univ. Press, Cambridge 1994. Go to original source...
  57. Macler B.A.: Salinity effects on photosynthesis, carbon allocation, and nitrogen assimilation in the red alga, Gelidium coulteri.-Plant Physiol. 88: 690-694, 1988. Go to original source...
  58. Madronich S.: Implications of recent total atmospheric ozone measurements for biological active ultraviolet radiation reaching the Earth's surface.-Geophys. Res. Let. 19: 37-40, 1992. Go to original source...
  59. Maia J.M., Ferreira-Silva S.L., Voigt E.L. et al.: [Activity of antioxidant enzymes and inhibition of root growth of cowpea under different levels of salinity.]-Acta Bot. Bras. 26: 342-349, 2012. [In Portuguese]
  60. Mallick N., Mohn F.H.: Reactive oxygen species: response of algal cells.-J. Plant Physiol. 157: 183-193, 2000. Go to original source...
  61. Mandal S.K., Ajay G., Monisha N. et al.: Differential response of varying temperature and salinity regimes on nutrient uptake of drifting fragments of Kappaphycus alvarezii: implication on survival and growth.-J. Appl. Phycol. 27: 1571-1581, 2015. Go to original source...
  62. McCready R.M., Guggolz A., Silveira V. et al.: Determination of starch and amylase in vegetables; application to peas.-Anal. Chem. 22: 1156-1158, 1950. Go to original source...
  63. Mendes L.F., Zambotti-Villela L., Colepicolo P. et al.: Metal cation toxicity in the alga Gracilaria domingenses as evaluated by the daily growth rates in synthetic seawater.-J. Appl. Phycol. 25: 1939-1947, 2013.
  64. Mitchell D.L., Jen J., Cleaver J.E.: Sequence specificity of cyclobutane pyrimidine dimers in DNA treated with solar (ultraviolet-B) radiation.-Nucleic Acids Res. 20: 225-229, 1992. Go to original source...
  65. Mittova V., Guy M., Tal M. et al.: Salinity up-regulates the antioxidative system in root mitochondria and peroxisomes of the wild salt-tolerant tomato species Lycopersicon pennellii.-J. Exp. Bot. 55: 1105-1113, 2004. Go to original source...
  66. Mittler R., Vanderauwera S., Suzuki N. et al.: ROS signalling: The new wave?-Trends Plant Sci. 16: 300-309, 2011. Go to original source...
  67. Mosmann T.: Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays.-J. Immunol. Methods 65: 55-63, 1983. Go to original source...
  68. Murphy J., Riley J.P.: A modified single solution method for the determination of phosphate in natural waters.-Anal. Chim. Acta 27: 31-36, 1962. Go to original source...
  69. Navarro N.P., Mansilla A., Plastino E.M.: Iridaea cordata (Gigartinales, Rhodophyta): responses to artificial UVB radiation.-J. Appl. Phycol. 22: 385-394, 2010. Go to original source...
  70. Navarro N.P., Mansilla A., Figueroa F.L. et al.: Short-term effects of solar UVradiation and NO3- supply on the accumulation of mycosporine-like amino acids in Pyropia columbina (Bangiales, Rhodophyta) under spring ozone depletion in the sub-Antarctic region.-Chile Bot. Mar. 57: 9-20, 2014. Go to original source...
  71. Nawkar G.M., Maibam P., Park J.H. et al.: UV-induced cell death in plants.-Int. J. Mol. Sci. 14: 1608-1628, 2013. Go to original source...
  72. Nejrup L.B., Pedersen M.F.: The effect of temporal variability in salinity on the invasive red alga Gracilaria vermiculophylla.-Eur. J. Phycol. 47: 254-263, 2012. Go to original source...
  73. Nitschke U., Karsten U., Eggert A.: Physiological performance of the red alga Stylonema alsidii (Stylonematophyceae) under varying salinities.-J. Exp. Mar. Biol. Ecol. 460: 170-176, 2014.
  74. Penniman C.A., Mathieson A.C., Penniman C.E.: Reproductive phenology and growth of Gracilaria tikvahien McLachlan (Gigartiales, Rhodophyta) in the Great Bay Estuary, New Hampshire.-Bot. Mar. 29: 147-154, 1986. Go to original source...
  75. Pereira D.T., Schmidt E.C., Bouzon Z.L. et al.: The effects of ultraviolet radiation-B response on the morphology, ultrastructure, and photosynthetic pigments of Laurencia catarinensis and Palisada flagellifera (Ceramiales, Rhodophyta): a comparative study.-J. Appl. Phycol. 26: 2443-2452, 2014. Go to original source...
  76. Pérez-Rodríguez E., Gómez I., Karsten U., Figueroa F.L.: Effects of UV radiation on photosynthesis and excretion of UVabsorbing compounds of Dasycladus vermicularis (Dasycladales, Chlorophyta) from southern Spain.-Phycologia 37: 379-387, 1998. Go to original source...
  77. Polo L.K., Feliz M.R., Kreusch M. et al.: Photoacclimation responses of the brown macroalga Sargassum Cymosum to the combined influence of UV radiation and salinity: cytochemical and ultrastructural organization and photosynthetic performance.-J. Photoch. Photobio. 90: 560-573, 2014. Go to original source...
  78. Polo L.K., Felix M.R., Kreusch M. et al.: Metabolic profile of the brown macroalga Sargassum cymosum (Phaeophyceae, Fucales) under laboratory UVradiation and salinity conditions.-J. Appl. Phycol. 27: 887-899, 2015. Go to original source...
  79. Poppe F., Hanelt D., Wiencke C.: Changes in ultrastructure, photosynthetic activity and pigments in the Antarctic red alga Palmaria decipiens during acclimation to UV radiation.-Bot. Mar. 45: 253-261, 2002. Go to original source...
  80. Poppe F., Schmidt R.A., Hanelt D. et al.: Effects of UVradiation on the ultrastructure of several red algae.-Phycol. Res. 51: 11-19, 2003.
  81. Rao M. V, Paliyath G., Ormrod P.: Ultraviolet-B- and ozoneinduced biochemical changes in antioxidant enzymes of Arabidopsis thaliana.-Plant Physiol. 110: 125-36, 1996. Go to original source...
  82. Recuenco-Muñoz L., Offre P., Valledor L. et al.: Targeted quantitative analysis of a diurnal RuBisCO subunit expression and translation profile in Chlamydomonas reinhardtii introducing a novel Mass Western approach.-J. Proteomics 113: 143-153, 2015. Go to original source...
  83. Rojas M.O.A.I., Neto J.J.C.G., Barbiere R.: [Physical-chemical evaluation of the water of the Jansen Lagoon, São Luis, MA.]-Acta Tecnol. 8: 19-24, 2013. [In Portuguese]
  84. Roleda M.T., Hanelt D., Kräbs G. et al.: Morphology, growth, photosynthesis and pigmentes in Laminaria ochroleuca (Laminariales, Phaeophyta) under ultraviolet radiation.-Phycology 43: 603-613, 2004. Go to original source...
  85. Scherner F., Ventura R., Barufi J.B., Horta P.A.: Salinity critical threshold values for photosynthesis of two cosmopolitan seaweed species: providing baselines for potential shifts on seaweed assemblages.-Mar. Environ. Res. 91: 14-25, 2013. Go to original source...
  86. Schmidt E.C., Scariot L.A., Rover T., Bouzon Z.L.: Changes in ultrastructure and histochemistry of two red macroalgae strains of Kappaphycus alvarezii (Rhodophyta, Gigartinales), as a consequence of ultraviolet B radiation exposure.-Micron 40: 860-869, 2009. Go to original source...
  87. Schmidt E.C., Nunes B.G., Maraschin M. et al.: Effect of ultraviolet-B radiation on growth, photosynthetic pigments, and cell biology of Kappaphycus alvarezii (Rhodophyta, Gigartinales) macroalgae brown strain.-Photosynthetica 48: 161-172, 2010. Go to original source...
  88. Schmidt E.C., dos Santos R.W., Faveri C. et al.: Response of the agarophyte Gelidium floridanum after in vitro exposure to ultraviolet radiation B: changes in ultrastructure, pigments, and antioxidant systems.-J. Appl. Phycol. 24: 1341-1352, 2012. Go to original source...
  89. Shannon J.C.: A procedure for the extraction and fractionation of carbohydrates from immature Zea mays kernels.-Res. Bull. 842: 1-8, 1968.
  90. Simioni C., Rover T, Schmidt E.C. et al.: Effects of brefeldin A on the endomembrane system and germ tube formation of the tetraspore of Gelidium floridanum (Rhodophyta, Florideophyceae).-J. Phycol. 50: 577-586, 2014. Go to original source...
  91. Souza-Mosimann R.M., Laudares-Silva R., Talgatti D.M. et al.: The diatom flora in Conceição Lagoon, Florianópolis, SC, Brazil.-Insula Rev. Bot. Florianópolis 40: 25-54, 2011.
  92. Sutherland B.M., Takayanagi S., Sullivan J.H., Sutherland J.C.: Plant responses to changing environmental stress: cyclobutyl pyrimidine dimer repair in soybean leaves.-Photochem. Photobiol. 64: 464-468, 1996. Go to original source...
  93. Takagi M., Karseno, Yoshida T.: Effect of salt concentration on intracellular accumulation of lipids and triacylglyceride in marine microalgae Dunaliella cells.-J. Biosci. Bioeng. 101: 223-226, 2006. Go to original source...
  94. Umbreit W.W., Burris R.H.: Method for Glucose Determination and other Sugars. Manome-tric Techniques, 4th ed. Pp. 338. Burgess Publishing Co., London 1964.
  95. van de Poll W.H., Hanelt D., Hoyer K. et al.: Ultraviolet-Binduced cyclobutane-pyrimidine dimer formation and repair in arctic marine macrophytes.-Photochem. Photobiol. 76: 493-500, 2002. Go to original source...
  96. Wang C., Mingyan W., Jingyu S. et al.: Research on the chemical constituents of Acanthophora spicifera in the South China Sea.-Chin. J. Magn. Reson. 15: 237-242, 1998.
  97. Wiencke C., ómez I., Pakker H. et al.: Impact of UVradiation on viability, photosynthetic characteristics and DNA on algal zoospores: implications for depth zonation.-Mar. Ecol. Progr. Ser. 197: 217-219, 2000. Go to original source...
  98. Yao N., Eisfelder B.J., Marvin J. et al.: The mitochondrion-an organelle commonly involved in programmed cell death in Arabidopsis thaliana.-Plant J. 40: 596-610, 2004. Go to original source...
  99. Zakaria N.A., Darah I., Shaida F.S. et al.: Phytochemical composition and antibacterial potential of hexane extract from malaysian red algae, Acanthophora spicifera (Vahl) Borgesen.-World Appl. Sci. J. 15: 496-501, 2011.
  100. Zhao J., Li L.: Effects of UV-B irradiation on isoforms of antioxidant enzymes and their activities in red alga Grateloupia filicina (Rhodophyta).-Chin. J. Oceanol. Limnol. 32: 1364-1372, 2014. Go to original source...
  101. Zeng L.M., Chao-Jie W., Jing-Yu S. et al.: Flavonoids from the red alga Acanthophora spicifera.-Chin. J. Chem. 19: 1097-1100, 2001.