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Effects of Natural Radiation, Photosynthetically Active Radiation and Artificial Ultraviolet Radiation-B on the Chloroplast Organization and Metabolism of Porphyra acanthophora var. brasiliensis (Rhodophyta, Bangiales)

Published online by Cambridge University Press:  16 November 2012

Zenilda L. Bouzon
Affiliation:
Central Laboratory of Electron Microscopy, Federal University of Santa Catarina88049-900, CP 476, Florianópolis, SC, Brazil
Fungyi Chow
Affiliation:
Institute of Bioscience, University of São Paulo05508-090, São Paulo, SP, Brazil
Carmen S. Zitta
Affiliation:
Post-Graduate Program in Cell Biology and Development, Department of Cell Biology, Embryology and Genetics, Federal University of Santa Catarina88049-900, CP 476, Florianópolis, SC, Brazil
Rodrigo W. dos Santos
Affiliation:
Post-Graduate Program in Cell Biology and Development, Department of Cell Biology, Embryology and Genetics, Federal University of Santa Catarina88049-900, CP 476, Florianópolis, SC, Brazil
Luciane C. Ouriques
Affiliation:
Post-Graduate Program in Cell Biology and Development, Department of Cell Biology, Embryology and Genetics, Federal University of Santa Catarina88049-900, CP 476, Florianópolis, SC, Brazil
Marthiellen R. de L. Felix
Affiliation:
Department of Botany, Federal University of Santa Catarina88010-970, CP 476, Florianópolis, SC, Brazil
Luz K.P. Osorio
Affiliation:
Department of Botany, Federal University of Santa Catarina88010-970, CP 476, Florianópolis, SC, Brazil
Claudiane Gouveia
Affiliation:
Department of Botany, Federal University of Santa Catarina88010-970, CP 476, Florianópolis, SC, Brazil
Roberta de Paula Martins
Affiliation:
Laboratory of Bioenergetic and Oxidative Stress, Department of Biochemistry, Federal University of Santa Catarina88049-900, CP 476, Florianópolis, SC, Brazil
Alexandra Latini
Affiliation:
Laboratory of Bioenergetic and Oxidative Stress, Department of Biochemistry, Federal University of Santa Catarina88049-900, CP 476, Florianópolis, SC, Brazil
Fernanda Ramlov
Affiliation:
Plant Morphogenesis and Biochemistry Laboratory, Federal University of Santa Catarina88049-900, CP 476, Florianópolis, SC, Brazil
Marcelo Maraschin
Affiliation:
Plant Morphogenesis and Biochemistry Laboratory, Federal University of Santa Catarina88049-900, CP 476, Florianópolis, SC, Brazil
Eder C. Schmidt*
Affiliation:
Post-Graduate Program in Cell Biology and Development, Department of Cell Biology, Embryology and Genetics, Federal University of Santa Catarina88049-900, CP 476, Florianópolis, SC, Brazil
*
*Corresponding author. E-mail: [email protected]
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Abstract

We undertook a study of Porphyra acanthophora var. brasiliensis to determine its responses under ambient conditions, photosynthetically active radiation (PAR), and PAR+UVBR (ultraviolet radiation-B) treatment, focusing on changes in ultrastructure, and cytochemistry. Accordingly, control ambient samples were collected in the field, and two different treatments were performed in the laboratory. Plants were exposed to PAR at 60 μmol photons m−2 s−1 and PAR + UVBR at 0.35 W m−2 for 3 h per day during 21 days of in vitro cultivation. Confocal laser scanning microscopy analysis of the vegetative cells showed single stellate chloroplast in ambient and PAR samples, but in PAR+UVBR-exposed plants, the chloroplast showed alterations in the number and form of arms. Under PAR+UVBR treatment, the thylakoids of the chloroplasts were disrupted, and an increase in the number of plastoglobuli was observed, in addition to mitochondria, which appeared with irregular, disrupted morphology compared to ambient and PAR samples. After UVBR exposure, the formation of carpospores was also observed. Plants under ambient conditions, as well as those treated with PAR and PAR+UVBR, all showed different concentrations of enzymatic response, including glutathione peroxidase and reductase activity. In summary, the present study demonstrates that P. acanthophora var. brasiliensis shows the activation of distinct mechanisms against natural radiation, PAR and PAR+UVBR.

Type
Biological Applications
Copyright
Copyright © Microscopy Society of America 2012

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Footnotes

Zenilda L. Bouzon and Eder C. Schmidt should be considered as first authors.

References

Aguilera, J., Dummermuth, A., Karsten, U., Schriek, R. & Wiencke, C. (2001). Enzymatic defences against photooxidative stress induced by ultraviolet radiation in Arctic marine macroalgae. Polar Biol 25, 432441.CrossRefGoogle Scholar
Bischof, K., Gómez, I., Molis, M., Hanelt, D., Karsten, U., Lüder, U., Roleda, M.Y., Zacher, K. & Wiencke, C. (2006). Ultraviolet radiation shapes seaweed communities. Rev Environ Sci Biotechnol 5, 141166.CrossRefGoogle Scholar
Bischof, K. & Steinhoff, F. (2012). Impacts of stratospheric ozone depletion and solar UVB radiation on seaweeds. In Seaweed Biology, Wiencke, C. & Bischof, K. (Eds.), pp. 433448. Berlin: Springer.CrossRefGoogle Scholar
Carlberg, I. & Mannervik, B. (1985). Glutathione reductase assay. Methods Enzymol 113, 484495.CrossRefGoogle Scholar
Cassina, A. & Radi, R. (1996). Differential inhibitory action of nitric oxide and peroxynitrite on mitochondrial electron transport. Arch Biochem Biophys 328, 309316.CrossRefGoogle ScholarPubMed
Costa, H., Gallego, S.M. & Tomaro, M.L. (2002). Effect of UV-B radiation on antioxidant defense system in sunflower cotyledons. Plant Sci 162, 939945.CrossRefGoogle Scholar
Edwards, P. (1970). Illustrated guide to the seaweeds and sea grasses in the vicinity of Porto Aransas, Texas. Contrib Mar Sci 15, 1228.Google Scholar
Eswaran, K., Subba Rao, P.V. & Mairh, O.P. (2001). Impact of ultraviolet-B radiation on Kappaphycus alvarezii (Solieraceae, Rhodophyta). Indian J Mar Sci 30, 105107.Google Scholar
Graham, L.E., Graham, J.M. & Wilcox, L.W. (2009). Algae, 2nd ed. San Francisco, CA: Pearson Education.Google Scholar
Grossman, A.R., Schaefer, M.R., Chiang, G.G. & Collier, J.L. (1993). The phycobilisome a light harvesting complex responsive to environmental conditions. Microbiol Rev 57, 725749.CrossRefGoogle ScholarPubMed
Hepler, P.K. & Gunning, B.E.S. (1998). Confocal fluorescence microscopy of plant cells. Protoplasma 201, 121157.CrossRefGoogle Scholar
Hiscox, J.D. & Israelstam, G.F. (1979). A method for the extraction of chlorophyll from leaf tissue without maceration. Can J Botany 57, 13321334.CrossRefGoogle Scholar
Holzinger, A., Karsten, U., Lütz, C. & Wiencke, C. (2006). Ultrastructure and photosynthesis in the supralittoral green macroalga Prasiola crispa from Spitsbergen (Norway) under UV exposure. Phycologia 45, 168177.CrossRefGoogle Scholar
Holzinger, A. & Lütz, C. (2006). Algae and UV irradiation: Effects on ultrastructure and related metabolic functions. Micron 37, 190207.CrossRefGoogle ScholarPubMed
Holzinger, A., Lütz, C., Karsten, U. & Wiencke, C. (2004). The effect of ultraviolet radiation on ultrastructure and photosynthesis in the red macroalgae Palmaria palmata and Odonthalia dentata from Artic waters. Plant Biol 6, 568577.CrossRefGoogle Scholar
Holzinger, A., Roleda, M.Y. & Lütz, C. (2009). The vegetative arctic freshwater green alga Zygnema is insensitive to experimental UV exposure. Micron 40, 831838.CrossRefGoogle ScholarPubMed
Hulshof, P.J.M., Kosmeijer-Schuil, T., West, C.E. & Hollman, P.C.H. (2007). Quick screening of maize kernels for provitamin A content. J Food Comp Anal 20, 655661.CrossRefGoogle Scholar
Karsten, U. & Wiencke, C. (1999). 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, 407415.CrossRefGoogle Scholar
Karsten, U., Wulff, A., Roleda, M.Y., Muller, R., Steinoff, F., Fredersdorf, J. & Wiencke, C. (2011). Physiological responses of polar benthic algae to ultraviolet radiation. In Biology of Polar Benthic Algae, Wiencke C. (Ed.), pp. 271297. Berlin: de Gruyter.Google Scholar
Kerr, J.B. & McElroy, C.T. (1993). Evidence for large upward trends of ultraviolet-B radiation linked to ozone depletion. Science 262, 10321034.CrossRefGoogle ScholarPubMed
Kim, Y.K., Guo, Q. & Packer, L. (2002). Free radical scavenging activity of red ginseng aqueous extracts. Toxicology 172, 149156.CrossRefGoogle ScholarPubMed
Kuhnen, S., Lemos, P.M.M., Campestrini, L.H., Ogliari, J.B., Dias, P.F. & Maraschin, M. (2009). Antiangiogenic properties of carotenoids: A potential role of maize as functional food. J Funct Foods 1, 284290.CrossRefGoogle Scholar
Kursar, T.A., van Der Meer, J. & Alberte, R.S. (1983). Light-harvesting system of the red alga Gracilaria tikvahiae, I. Biochemical analyses of pigment mutations. Plant Phys 73, 353360.CrossRefGoogle ScholarPubMed
Latini, A., Rodriguez, M. & Borba, R.R. (2005). 3-Hydroxyglutaric acid moderately impairs energy metabolism in brain of young rats. Neuroscience 135, 111120.CrossRefGoogle ScholarPubMed
Lesser, M.P. & Shick, J.M. (1994). Effects of irradiance and ultraviolet radiation on photoadaptation in the zooxanthellae of Aiptasia pallida: Primary production, photoinhibition, and enzymic defenses against oxygen toxicity. Marine Biol 102, 243255.CrossRefGoogle Scholar
Lowry, O.H., Rosebough, N.G. & Farr, A.L. (1951). Protein measurement with the folin phenol reagent. J Biol Chem 193, 265275.CrossRefGoogle ScholarPubMed
Madronich, S. (1992). Implications of recent total atmospheric ozone measurements for biological active ultraviolet radiation reaching the Earths surface. Geophys Res Lett 19, 3740.CrossRefGoogle Scholar
Mitchell, D.L., Jen, J. & Cleaver, J.E. (1992). Sequence specificity of cyclobutane pyrimidine dimers in DNA treated with solar (ultraviolet B) radiation. Nucl Acids Res 20, 225229.CrossRefGoogle ScholarPubMed
Navarro, N.P., Mansilla, A. & Palacios, M. (2008). UVB effects on early developmental stages of commercially important macroalgae in southern Chile. J Appl Phycol 20, 897906.CrossRefGoogle Scholar
Navarro, N.P., Mansilla, A. & Plastino, E.M. (2010). Iridaea cordata (Gigartinales, Rhodophyta): Responses to artificial UVB radiation. J Appl Phycol 22, 385394.CrossRefGoogle Scholar
Oliveira, E.C. (1977). Algas marinhas bentônicas do Brasil. Thesis. São Paulo, Brazil: University of São Paulo. Google Scholar
Oliveira, E.C. & Coll, J. (1975). The genus Porphyra C. Ag. (Rhodophyta-Bangiales) in the American South Atlantic. I. Brazilian species. Bot Mar 18, 191197.Google Scholar
Pavia, H., Cervin, G., Lindgren, A. & Aberg, P. (1997). Effects of UV-B radiation and simulated herbivory on phlorotannins in the brown alga Ascophyllum nodosum . Marine Ecol Prog Ser 157, 139146.CrossRefGoogle Scholar
Penniman, C.A., Mathieson, A.C. & Penniman, C.E. (1986). Reproductive phenology and growth of Gracilaria tikvahiae McLachlan (Gigartinales, Rhodophyta) in the Great Bay Estuary, New Hampshire. Bot Mar 29, 147154.CrossRefGoogle 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, 253261.CrossRefGoogle Scholar
Poppe, F., Schmidt, R.A.M., Hanelt, D. & Wiencke, C. (2003). Effects of UV radiation on the ultrastructure of several red algae. Phycol Res 51, 1119.CrossRefGoogle Scholar
Reynolds, E.S. (1963). The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. J Cell Biol 17, 208212.CrossRefGoogle ScholarPubMed
Roleda, M., Campana, G., Wiencke, C., Hanelt, D., Quartino, M.L. & Wulff, A. (2009). Sensitivity of Antarctic Urospora penicilliformis (Ulotrichales, Chlorophyta) to ultraviolet radiation is life stage dependent. J Phycol 45, 600609.CrossRefGoogle ScholarPubMed
Roleda, M.Y., Lütz-Meindl, U., Wiencke, C. & Lütz, C. (2010). Physiological, biochemical, and ultrastructural responses of the green macroalga Urospora penicilliformis from Arctic Spitsbergen to UV radiation. Protoplasma 243, 105116.CrossRefGoogle ScholarPubMed
Roleda, M.Y., van de Poll, W.H., Wiencke, C. & Hanelt, D. (2004). PAR and UVBR effects on photosynthesis, viability, growth and DNA in different life stages of two coexisting Gigartinales: Implications for recruitment and zonation pattern. Marine Ecol Prog Ser 281, 3750.CrossRefGoogle Scholar
Schmidt, E.C., Maraschin, M. & Bouzon, Z.L. (2010a). Effects of UVB radiation on the carragenophyte Kappaphycus alvarezii (Rhodophyta, Gigartinales): Changes in ultrastructure, growth, and photosynthetic pigments. Hydrobiologia 649, 171182.CrossRefGoogle Scholar
Schmidt, E.C., Nunes, B.G., Maraschin, M. & Bouzon, Z.L. (2010b). Effect of ultraviolet-B radiation on growth, photosynthetic pigments, and cell biology of Kappaphycus alvarezii (Rhodophyta, Gigartinales) macroalgae brown strain. Photosynthetica 48, 161172.CrossRefGoogle Scholar
Schmidt, E.C., Pereira, B., Mansur-Lessa, C., Santos, R., Scherner, F., Horta, P.A., Martins, R.P., Latini, A., Maraschin, M. & Bouzon, Z.L. (2012a). Alterations in architecture and metabolism induced by ultraviolet radiation-B in the carragenophyte Chondracanthus teedei (Rhodophyta, Gigartinales). Protoplasma 249, 353367.CrossRefGoogle ScholarPubMed
Schmidt, E.C., Pereira, B., Santos, R., Gouveia, C., Costa, G.B., Faria, G.S.M., Scherner, F., Horta, P.A., Paula, M.R., Latini, A., Ramlov, F., Maraschin, M. & Bouzon, Z.L. (2012b). Responses of the macroalgae Hypnea musciformis after in vitro exposure to UV-B. Aquat Bot 100, 817.CrossRefGoogle Scholar
Schmidt, E.C., Santos, R., Faveri, C., Horta, P.A., Paula, M.R., Latini, A., Ramlov, F., Maraschin, M. & Bouzon, Z.L. (2012c). Response of the agarophyte Gelidium floridanum after in vitro exposure to ultraviolet radiation B: Changes in ultrastructure, pigments, and antioxidant systems. J Appl Phycol DOI 10.1007/s10811-012-9786-4. CrossRefGoogle Scholar
Schmidt, E.C., Santos, R., Horta, P., Maraschin, M. & Bouzon, Z.L. (2010c). Effects of UVB radiation on the agarophyte Gracilaria domingensis (Rhodophyta, Gracilariales): Changes in cell organization, growth and photosynthetic performance. Micron 41, 919930.CrossRefGoogle ScholarPubMed
Schmidt, E.C., Scariot, L.A., Rover, T. & Bouzon, Z.L. (2009). 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, 860869.CrossRefGoogle ScholarPubMed
Scott, C.E. & Eldridge, A.L. (2005). Comparison of carotenoid content in fresh, frozen and, canned corn. J Food Comp Anal 18, 551559.CrossRefGoogle Scholar
Shiu, C.T. & Lee, T.M. (2005). Ultraviolet-B-induced oxidative stress and responses of the ascorbate-glutathione cycle in a marine macroalga Ulva fasciata . J Exp Bot 56, 28512865.CrossRefGoogle Scholar
Steinhoff, F.S., Wiencke, C., Müller, R. & Bischof, K. (2008). Effects of ultraviolet radiation and temperature on the ultrastructure of zoospores of the brown macroalga Laminaria hyperborean . Plant Biol 10, 388397.CrossRefGoogle Scholar
Talarico, L. (1996). Phycobiliproteins and phycobilisomes in red algae: Adaptive responses to light. Sci Mar 60, 205222.Google Scholar
Vosjan, J., Döhler, H. & Nieuwlan, G. (1990). Effect of UV-B irradiance on the ATP content of microorganisms of the Weddell Sea (Antarctica). Neth J Sea Res 25, 391394.CrossRefGoogle Scholar
Wellburn, A.R. (1994). 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, 307313.CrossRefGoogle Scholar
Wendel, A. (1981). Glutathione peroxidase. Method Enzymol 77, 325333.CrossRefGoogle ScholarPubMed
Wood, W.F. (1989). Photoadaptive responses of the tropical red alga Eucheuma striatum Schmitz (Gigartinales) to ultra-violet radiation. Aquat Bot 33, 4151.CrossRefGoogle Scholar
Yakovleva, I.M. & Titlyanov, E.A. (2001). Effect of high visible and UV irradiance on subtidal Chondrus crispus: Stress, photoinhibition and protective mechanism. Aquat Bot 71, 4761.CrossRefGoogle Scholar
Zacarias, A.A., Moresco, H.H., Horst, H., Brighente, I.M.C., Marques, M.C.A & Pizzollati, M.G. (2007). Determinação do teor de fenólicos e flavonóides no extrato e frações de Tabebuia heptaphylla. 30a Reunião Anual da Sociedade Brasileira de Química, Santa Maria, Rio Grande do Sul. Google Scholar
Zacher, K., Roleda, M.Y., Wulff, A., Hanelt, D. & Wiencke, C. (2009). Responses of Antarctic Iridaea cordata (Rhodophyta) tetraspores exposed to ultraviolet radiation. Phycol Res 57, 186193.CrossRefGoogle Scholar