Photosynthetica, 2010 (vol. 48), issue 2

Photosynthetica 2010, 48(2):161-172 | DOI: 10.1007/s11099-010-0022-7

Effect of ultraviolet-B radiation on growth, photosynthetic pigments, and cell biology of Kappaphycus alvarezii (Rhodophyta, Gigartinales) macroalgae brown strain

É. C. Schmidt1,*, B. G. Nunes2, M. Maraschin3, Z. L. Bouzon1,4
1 Department of Cell Biology, Embryology and Genetics, Federal University of Santa Catarina, SC Florianópolis, Brazil
2 Department of Aquaculture, Federal University of Santa Catarina, SC Florianópolis, Brazil
3 Plant Morphogenesis and Biochemistry Laboratory, Federal University of Santa Catarina, SC Florianópolis, Brazil
4 Central Laboratory of Electron Microscopy, Federal University of Santa Catarina, SC Florianópolis, Brazil

Kappaphycus alvarezii is a seaweed of great economic importance for the extraction of kappa carrageenan from its cell walls. The most common strains are dark red, brown, yellow, and different gradations of green. It is known that ultraviolet radiation (UVR) affects macroalgae in many important ways, including reduced growth rate, reduction of primary productivity, and changes in cell biology and ultrastructure. Therefore, we examined the brown strain of K. alvarezii exposed to ultraviolet-B radiaton (UVBR) for 3 h per day during 28 days of cultivation. The control plants showed growth rates of 7.27% d-1, while plants exposed to UVBR grew only 4.0% d-1. Significant differences in growth rates and in phycobiliproteins between control and exposed plants were also found. Compared with control plants, phycobiliprotein contents were observed to decrease after UV-B exposure. Furthermore, the chlorophyll a (Chl a) contents decreased and showed significant differences. UVBR also caused changes in the ultrastructure of cortical and subcortical cells, which included increased thickness of the cell wall and number of plastoglobuli, reduced intracellular spaces, changes in the cell contour, and destruction of chloroplast internal organization. Reaction with Toluidine Blue showed an increase in the thickness of the cell wall, and Periodic Acid-Schiff stain showed a decrease in the number of starch grains. By the significant changes in growth rates, photosynthetic contents and ultrastructual changes observed, it is clear that UVBR negatively affects intertidal macroalgae and, by extension, their economic viability.

Keywords: brown strain of Kappaphycus alvarezii; chloroplast; growth rates; photosynthetic pigments; ultrastructure; ultraviolet-B radiation

Received: October 19, 2009; Accepted: February 6, 2010; Published: June 1, 2010Show citation

ACS AIP APA ASA Harvard Chicago IEEE ISO690 MLA NLM Turabian Vancouver
Schmidt, É.C., Nunes, B.G., Maraschin, M., & Bouzon, Z.L. (2010). Effect of ultraviolet-B radiation on growth, photosynthetic pigments, and cell biology of Kappaphycus alvarezii (Rhodophyta, Gigartinales) macroalgae brown strain. Photosynthetica48(2), 161-172. doi: 10.1007/s11099-010-0022-7.
Download citation

References

  1. Aguilera, J., Karsten, U., Lippert, H., Vögele, B., Philipp, E., Hanelt, D., Wiencke, C.: Effects of solar radiation on growth, photosynthesis and respiration of macroalgae from the Arctic. - Mar. Ecol. Progress Ser. 191: 109-119, 1999. Go to original source...
  2. Aguirre-von-Wobeser, E., Figueroa, F.L., Cabello-Pasini, A.: Photosynthesis and growth of red and green morphotypes of Kappaphycus alvarezii (Rhodophyta) from the Philippines. - Mar. Biol. 138: 679-686, 2001. Go to original source...
  3. Altamirano, M., Flores-Moya, A., Figueroa, F.L., 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: 119-126, 2000. Go to original source...
  4. Areces, A.J.: [Commercial cultivation of carrageenophytes genera Kappaphycus Doty.] - In: Alveal, K., Ferrario, M.E., Oliveira, E.C., Sar, E. (ed.): Phycologycal Methods Manual. Pp. 529-549. University of Concepción, Concepción 1995. [In Spanish]
  5. Aro, E.-M., Virgen, I., Andersson, B.: Photoinhibition of Photosystem II. Inactivation, protein damage and turnover. - Biochim. Biophys. Acta 1143: 113-134, 1993. Go to original source...
  6. Beach, K.S., Smith, C.M., Okano, R.: Experimental analysis of rhodophyte photoacclimation to PAR and UV-radiation using in vivo absorbance spectroscopy. - Bot. Mar. 43: 525-536, 2000. Go to original source...
  7. Bischof, K., Hanelt, D., Wiencke, C.: Effects of ultraviolet radiation on photosynthesis and related enzyme reactions of marine macroalgae. - Planta 211: 555-562, 2000. Go to original source...
  8. Bornmann, J. F., Teramura, A. H.: Effects of ultraviolet-B radiation on terrestrial plants. - In: Young, A.R., Björn, L.O., Moan, J., Nultsch, W. (ed.). Environmental UV Photobiology. Pp. 427-471. Plenum Press, New York - London 1993. Go to original source...
  9. Bouzon, Z.L.: Histochemistry and ultrastructure of the ontogenesis of the tetrasporangia of Hypnea musciformis (Wulfen) J. V. Lamour. (Gigartinales, Rhodophyta). - Rev. Bra. Bot. 29: 229-238, 2006. [In Portuguese] Go to original source...
  10. Bowler, C., van Montagu, M., Inzé, D.: Supeoxide dismutase and stress tolerance. - Annu. Rev. Plant Physiol. Plant Mol. Biol. 43: 83-116, 1992. Go to original source...
  11. Buma, A.G.J., van Hannen, E.J., Roza, L., Veldhuis, M.J.W., Gieske, W.W.C.: Monitoring ultraviolet-B-induced DNA damage in individual diatom cells by immunofluorescent thymine dimer detection. - J. Phycol. 31: 314-321, 1995. Go to original source...
  12. Buma, A.G.J., van Oijen, T., van de Poll, W., Veldhuis, M.J.W., Gieskes, W.W.C.: The sensitivity of Emiliania huxleyi (Prymnesiophyceae) to ultraviolet-B radiation. - J. Phycol. 36: 296-303, 2000. Go to original source...
  13. Chow, W.S., Strid, A., Anderson, J.M.: Short-term treatment of pea plants with supplementary Ultraviolet-B radiation: Recovery time-courses of some photosynthetic functions and components. - In: Murata, N, (ed.).: Research in Photosynthesis. Pp. 361-364. Kluwer Academic Publishing, Dordrecht 1992.
  14. Doty, M.S., Caddy, J.F., Santelices, B.: The production and use of Eucheuma. - In: Doty, M.S., Caddy, J.F., Santelices, B. (ed.): Case Studies of Seven Commercial Seaweed Resources. Pp. 123-164. FAO United Nations Fisheries Technical Paper, Rome 1987.
  15. Doughty, C.J., Hope, A.B.: Effects of ultraviolet radiation on the membranes of Chara corallina. - Membr. Biol. 13: 185-198, 1973. Go to original source...
  16. Edwards, P.: Illustrated guide to the seaweeds and sea grasses in the vicinity of Porto Arkansas, Texas. - Contr. Mar. Sci. 15: 1-228, 1970.
  17. Eswaran, K., Subba Rao, P.V., Mairh, O.P.: Impact of ultraviolet-B radiation on Kappaphycus alvarezii (Solieraceae, Rhodophyta). - Indian J. Mar. Sci. 30: 105-107, 2001.
  18. Eswaran, K., Mairh, O.P., Subba Rao, P.V.: Inhibition of pigments and phycocolloid in a marine red algae Gracilaria edulis by ultraviolet-B radiation. - Biol. Plant. 45: 157-159, 2002. Go to original source...
  19. Franklin, L.A., Forster, R.M.: The changing irradiance environment: consequences for marine macrophyte physiology, productivity and ecology. - Eur. J. Phycol. 32: 207-232, 1997. Go to original source...
  20. Gantt, E.: Phycobilisomes. - Annu. Rev. Plant Physiol. 32: 327-347, 1981. Go to original source...
  21. Gahan, P.B.: Plant Histochemistry and Cytochemistry: An Introduction. - Academic Press, London 1984.
  22. Gallo, R.L., Kochevar, I.E., Granstein, R.D.: Ultraviolet radiation induces a change in cell membrane potential in vitro: a possible signal for ultraviolet radiation induced alteration in cell activity. - J. Photochem. Photobiol. 49: 655-662, 1989. Go to original source...
  23. Garbary, D.J., Kim, K.Y., Hoffman, J.: Cytological damage to the red alga Griffithsia pacifica from ultraviolet radiation. - Hydrobiologia 512: 165-170, 2004. Go to original source...
  24. Gerber, S., Häder D.P.: Effect of solar irradiation on motility and pigmentation of three species of phytoplankton. - Environ. Exp. Bot. 33: 515-521, 1993. Go to original source...
  25. Gordon, E.M., McCandless, E.L.: Ultrastructure and histochemistry of Chondrus crispus Stackhouse. - In: Harvey, M.J., McLachlan, J. (ed.): Chondrus Crispus. Pp. 111-133. Nova Scotian Institute Science, Halifax 1973.
  26. Grossman, A. R., Schaefer, M.R., Chiang, G.G., Collier, J.L.: The phycobilisome a light harvesting complex responsive to environmental conditions. - Microbiol. Rev. 57: 725-749, 1993. Go to original source...
  27. Han, T., Kong, J.A., Han, Y. S., Kang, S.H., Häder, D.P.: UVA/blue light-induced reactivation of spore germination in UVB irradiated Ulva pertusa (Chlorophyta). - J. Phycol. 40: 315-322, 2004. Go to original source...
  28. Hideg, É., Vass, I.: UV-B induced free radical production in plant leaves and isolated thylakoid membranes. - Plant Sci. 115: 251-260. 1996. Go to original source...
  29. Hóllosy, F.: Effects of ultraviolet radiation on plant cells. - Micron 33: 179-197, 2002. Go to original source...
  30. Holzinger, A., Lütz, C., Karsten, U., Wiencke, C.: The effect of ultraviolet radiation on ultrasctruture and photosynthesis in the red macroalgae Palmaria palmata and Odonthalia dentata from Artic waters. - Plant Biol. 6: 568-577, 2004. Go to original source...
  31. Holzinger, A., Karsten, U., Lütz, C., Wiencke, C.: Ultrastructure and photosynthesis in the supralittoral green macroalga Prasiola crispa from Spitsbergen (Norway) under UV exposure. - Phycologia 45: 168-177, 2006. Go to original source...
  32. Holzinger, A., Lütz, C.: Algae and UV irradiation: Effects on ultrastructure and related metabolic functions. - Micron 37: 190-207, 2006. Go to original source...
  33. Iwanzik, W., Tevini, M., Dohnt, G., Voss, M.; Weiss, W.; Gräber, P.; Renger, G.: Action of UV-B radiation on photosynthetic primary reactions in spinach chloroplasts. - Physiol. Plant. 58: 401-407, 1983. Go to original source...
  34. Karentz, D., Cleaver, J.E., Mitchell, D.L.: DNA damage in the Antarctic. - Nature 350: 28, 1991. Go to original source...
  35. Karsten, U., Wiencke, C.: Factors controlling the formation of UV-absorbing mycosporine-like amino acids in the marine red alga Palmaria palmata from Spitsbergen (Norway). - J. Plant Physiol. 155: 407-415, 1999. Go to original source...
  36. Karsten, U., Bischof, K., Hanelt, D., Tüg, H., Wiencke, C.: The effect of ultraviolet radiation on photosynthesis and ultraviolet-absorbing substances in the endemic Arctic macroalga Devaleraea ramentacea (Rhodophyta). - Physiol. Plant 105: 58-66, 1999. Go to original source...
  37. Kerr, J.B., Mc Elroy, C. T.: Evidence for large upward trends of ultraviolet-B radiation linked to ozone depletion. - Science 262: 1032-1034, 1993. Go to original source...
  38. Kirchhoff, V.W.J.H., Schuch, N.J., Pinheiro, D.K., Harris, J.M.: Evidence for ozone hole perturbation at 30° South. - Atmospheric Environ. 30: 1481-1484, 1996. Go to original source...
  39. Kursar, T.A., van Der Meer, J., Alberte, R.S.: Light-harvesting system of the red alga Gracilaria tikvahiae. I. Biochemical analyses of pigment mutations. - Plant Physiol. 73: 353-360, 1983. Go to original source...
  40. Lão, K., Glaser, A.N.: Ultraviolet-B photodestruction of light-harvesting complex. - Proc. Nat. Acad. Sci. USA 93: 5258-5263, 1996. Go to original source...
  41. Lesser, M.P., Shick, J.M.: Effects of irradiance and ultraviolet radiation on photoadaptation in the zooxanthellae of Aiptasia pallida: primary production, photoinhibition, and enzymic defenses against oxygen toxicity. - Mar. Biol. 102: 243-255, 1994.
  42. Lubin, D., Jensen, E. H.: Effects of clouds and stratospheric ozone depletion on ultraviolet-radiation trends. - Nature 377: 710-713, 1995. Go to original source...
  43. Lütz, C., Seidlitz, H.K., Meindl, U.: Physiological and structural changes in the chloroplast of the green alga Micrasterias denticulata induced by UV-B simulation. - Plant Ecol. 128: 55-64, 1997. Go to original source...
  44. Madronich, S.: Implications of recent total atmospheric ozone measurements for biological active ultraviolet radiation reaching the Earths surface. - Geophys. Res. Lett. 19: 37-40, 1992. Go to original source...
  45. Meindl, U., Lütz, C.: Effects of UV irradiation on cell development and ultrastructure of green alga Micrasterias. - J. Photochem. Photobiol. B-Biol. 36: 285-292, 1996. Go to original source...
  46. 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...
  47. Murphy, T. M.: Membranes as targets of ultraviolet radiation. - Physiol. Plant 58: 381-388. 1983. Go to original source...
  48. Neale, P. J., Cullen, J. C., Lesser, M. P., Melis, A.: Physiological bases for detecting and predicting Photoinhibition of aquatic photosynthesis by PAR and UV radiation. - In: Yamamoto, H.Y., Smith, C.M. (ed.) Photosynthetic Responses to the Environment. Pp. 61-77. Amer. Soc. Plant Physiol. Rockville 1993.
  49. Oliveira, E.C.: Seaweed: A feature still little exploited by Brazil. - Panorama da Aqüicul. 7: 24-26, 1997. [In Portuguese]
  50. Pakker, H., Martins, R.S.T., Boelen, P., Buma, A.G.J., Nikaido, O., Breeman, A.M.: Effects of temperature on the photoreactivation of ultraviolet-b-induced DNA damage in Palmaria palmata (Rhodophyta). - J. Phycol. 36: 334-341, 2000. Go to original source...
  51. Pang, S., Gomez, I., Lüning, K.: The red macroalga Delesseria sanguinea as a UVB-sensitive model organism: selective growth reduction by UVB in outdoor experiments and rapid recording of growth rate during and after UV pulses. - Eur. J. Phycol. 36: 207-216, 2001. Go to original source...
  52. Paula, E.J., Pereira, R.T. L.: The "marinomia" mariculture of exotic seaweed Kappaphycus alvarezii to carrageenans produce in Brazil. - Panorama da Aqüicul. 8: 10-15, 1998. [In Portuguese]
  53. Penniman, C.A., Mathieson, A.C, Penniman C.E.: Reproductive phenology and growth of Gracilaria tikvahiae McLachlan (Gigartinales, Rhodophyta) in the Great Bay Estuary, New Hampshire. - Bot Mar. 29: 147-154, 1986. Go to original source...
  54. 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...
  55. Poppe, F., Schmidt, R.A.M., Hanelt, D., Wiencke, C.: Effects of UV radiation on the ultrastructure of several red algae. - Phycol. Res. 51: 11-19, 2003. Go to original source...
  56. Post, A., Gentle, S., Larkum, A.W.S.: Algal photosynthesis: inhibition by UV-B radiation, recovery and UV-absorbing pigments. - In: Murata, N. (ed.): Research in Photosynthesis. Pp. 847-850. Kluwer Academic Publ., Dordrecht - Boston - London 1992.
  57. Premkumar, A., Eswaran, K., Kulandaivelu, G.: Growth, biochemical and photosynthetic responses of greengram seedlings under water stress to ultraviolet-B radiation. - Plant Physiol. Biochem. 20: 31-35, 1993.
  58. Reis, R.P.: Caldeira, A.Q.: Miranda, A.P.S., Barros-Barreto, M.B.: Potencial of carrageenophyte mariculture Hypnea musciformis (Wulfen) J.V. Lamour. (Gigartinales - Rhodophyta) in Marambaia Island, BaÍa de Sepetiba, RJ, Brazil. - Acta Bot. Bras. 20: 763-769, 2006. [In Portuguese] Go to original source...
  59. Reynolds, E.S.: The use of lead citrate at light pH as an electron opaque stain in electron microscopy. - J. Cell. Biol. 17: 208-212, 1963. Go to original source...
  60. Rousseaux, M.C., Ballaré, C.L., Giordano, C.V., Scopel, A.L., Zima, A.M., Swarcberg-Bracchitta, M., Searles, P.S., Caldwell, M.M., Díaz, S.B.: Ozone depletion and UVB radiation: impact on plant DNA damage in southern South America. - Proc. Natl. Acad. Sci. USA 96: 15310-15315, 1999. Go to original source...
  61. Santee, M.L., Read, W.G., Waters, J.W., Froidevaux, L., Manney, G.L., Flower, D.A, Jarnot, R.F., Harwood, R.S., Peckham, G.E.: Interhemispheric differences in polar stratospheric HNO3, H2O, ClO, and O3. - Science 267: 849-852, 1995. Go to original source...
  62. Sinha, R.P., Lebert, M., Kumar, A., Kumar, H.D., Hader, D.P.: Spectroscopic and biochemical analyses of UV effects on phycobiliproteins of Anabaena sp and Nostoc carmium. - Bot. Acta 108: 87-92, 1995. Go to original source...
  63. Sommaruga, R.: The role of solar UV radiation in the ecology of alpine lakes. - J. Photochem. Photobiol. B-Biol. 62: 35-42, 2001. Go to original source...
  64. Sonntag, B., Summerer, M., Sommaruga, R.: Sources of mycosporine-like amino acids in planktonic Chlorella-bearing ciliates (Ciliophora). - Freshwater Biol. 52: 1476-1485, 2007. Go to original source...
  65. Staxén, I., Bornman, J.F.: A morphological and cytological study of Petunia hybrida exposed to UV-B radiation. - Physiol. Plant 91: 735-740, 1994. Go to original source...
  66. Steinhoff, F.S., Wiencke, C., Müller, R., Bischof, K.: Effects of ultraviolet radiation and temperature on the ultrastructure of zoospores of the brown macroalga Laminaria hyperborea. - Plant Biol. 10: 388-397, 2008. Go to original source...
  67. Strid, A., Chow, W.S., Anderson, J. M.: UV-B damage and protection at the molecular level in plants. - Photosynth. Res. 39: 475-489, 1994. Go to original source...
  68. Talarico, L.: Phycobiliproteins and phycobilisomes in red algae: Adaptive responses to light. - Sci. Mar. 60: 205-222, 1996.
  69. Talarico, L., Maranzana, G.: Light and adaptative responses in red macroalgae: an overview. - J. Photochem. Photobiol. B-Biol. 56: 1-11, 2000. Go to original source...
  70. van de Poll, W.H., Eggert, A., Buma, G.J., Breeman, A.M.: Effects of UV-B induced DNA damage and photoinhibition on growth of temperate marine red macrophytes: habitatrelated differences in UV-B tolerance. - J. Appl. Phycol. 37: 30-37, 2001. Go to original source...
  71. Vass, I.: Adverse effects of UV-B light on the structure and function of the photosynthetic apparatus. - In: Pessarakli, M. (ed.). Handbook of photosynthesis. Pp. 931-949. Marcel Dekker, New York - Basel - Hong Kong 1997.
  72. Wellburn, A.R.: The spectral determination of chlorophyll a and chlorophyll b, as well as total carotenoids, using various solvents with spectrophotometers of different resolution. - J. Plant Physiol. 144: 307-313, 1994. Go to original source...
  73. Wood, W.F.: Effect of solar ultraviolet radiation on the kelp Ecklonia radiata. - Mar. Biol. 96: 143-150, 1987. Go to original source...
  74. Wood, W.F.: Photoadaptive responses of the tropical red alga Eucheuma striatum Schmitz (Gigartinales) to ultra-violet radiation. - Aquat. Bot. 33: 41-5, 1989. Go to original source...
  75. Worrest, R.C.: Impact of solar ultraviolet-B radiation (290-320 nm) upon marine microalgae. - Physiol. Plant 58: 428-434, 1983. Go to original source...
  76. Yakovleva, I.M., Titlyanov, E. A.: Effect of high visible and UV irradiance on subtidal Chondrus crispus: stress, photo-inhibition and protective mechanism. - Aquat. Bot. 71: 47-61, 2001. Go to original source...