Skip to main content
Log in

Response of the agarophyte Gelidium floridanum after in vitro exposure to ultraviolet radiation B: changes in ultrastructure, pigments, and antioxidant systems

  • Published:
Journal of Applied Phycology Aims and scope Submit manuscript

Abstract

As a source of agar, the red macroalga Gelidium floridanum is a seaweed of great economic importance. However, it grows in a region exposed to high ultraviolet B radiation (UVBR). Therefore, to study the in vitro effect of UVBR on this plant, apical segments of G. floridanum were cultivated and exposed to photosynthetically active radiation (PAR) at 80 μmol photons m−2 s−1 and PAR + UVBR at 1.6 W m−2 at 3 h per day for 7 days. The samples were processed for electron microscopy, and agar yield, growth rates, mitochondrial activity, protein levels, chlorophyll a, phycobiliproteins, carotenoids and phenolic compounds, and photosynthetic performance were examined. After 7 days of exposure to PAR + UVBR, G. floridanum experienced ultrastructural damage that was primarily observed in the internal organization of chloroplasts, increased cell wall thickness, as well as increased volume of plastoglobuli and free ribosomes. Moreover, this exposure might have caused photodamage and photoinhibition of photosynthetic pigments (chlorophyll a and phycobiliproteins), leading to a decrease in photosynthetic efficiency, relative electron transport rate, and maximum photosynthetic rate. These phenomena were matched with a corresponding decrease in growth rates and depigmentation, combined with partial necrosis of the apical segments exposed to PAR + UVBR. Additionally, the UVBR-induced damage elicited a marked cellular antioxidant response, possibly as a consequence of free radical generation.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Abdala-Díaz RT, Cabello-Pasini A, Pérez-Rodríguez E, Conde Álvarez RM, Figueroa FL (2006) Daily and seasonal variations of optimum quantum yield and phenolic compounds in Cystoseira tamariscifolia (Phaeophyta). Mar Biol 148:459–465

    Article  Google Scholar 

  • 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 25:432–441

    Google Scholar 

  • Aro EM, Virgen I, Andersson B (1993) Photoinhibition of Photosystem II. Inactivation, protein damage and turnover. Biochim Biophy Acta 1143:113–134

    Article  CAS  Google Scholar 

  • Beach KS, Smith CM, Okano R (2000) Experimental analysis of rhodophyte photoacclimation to PAR and UV-radiation using in vivo absorbance spectroscopy. Bot Mar 43:525–536

    Article  CAS  Google Scholar 

  • Bischof K, Gómez I, Molis M, Hanelt D, Karsten U, Lüder U, Roleda MY, Zacher K, Wiencke C (2006) Ultraviolet radiation shapes seaweed communities. Rev Environ Sci Biotechnol 5:141–166

    Article  CAS  Google Scholar 

  • Bornmann JF, Teramura AH (1993) Effects of ultraviolet-B radiation on terrestrial plants. In: Young AR, Björn LO, Moan J, Nultsch W (eds) Environ UV photobiol. Plenum, New York, pp 427–471

    Google Scholar 

  • Bouzon ZL, Ouriques LC, Oliveira EC (2006) Spore adhesion and cell wall formation in Gelidium Floridanum (Rhodophyta, Gelidiales). J Appl Phycol 18:287–294

    Google Scholar 

  • Carlberg I, Mannervik B (1985) Glutathione reductase. Methods Enzimología 113:484–490

    Google Scholar 

  • Cassina A, Radi R (1996) Differential inhibitory action of nitric oxide and peroxynitrite on mitochondrial electron transport. Arch Biochem Biophys 328:309–316

    Google Scholar 

  • Chow WS, Strid A, Anderson JM (1992) 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. Kluwer Academic, Dordrecht, pp 361–364

    Google Scholar 

  • Costa H, Gallego SM, Tomaro ML (2002) Effect of UV-B radiation on antioxidant defense system in sunflower cotyledons. Plant Sci 162:939–945

    Article  CAS  Google Scholar 

  • Doughty CJ, Hope AB (1973) Effects of ultraviolet radiation on the membranes of Chara corallina. J Membr Biol 13:185–198

    Article  CAS  Google Scholar 

  • Edwards P (1970) Illustrated guide to the seaweeds and sea grasses in the vicinity of Port Aransas, Texas. Contr Mar Sci 15:1–228

    Google Scholar 

  • Eswaran K, Subba Rao PV, Mairh OP (2001) Impact of ultraviolet-B radiation on Kappaphycus alvarezii (Solieraceae, Rhodophyta). Indian J Mar Sci 30:105–107

    Google Scholar 

  • Eswaran K, Mairh OP, Subba Rao PV (2002) Inhibition of pigments and phycocolloid in a marine red algae Gracilaria edulis by ultraviolet-B radiation. Biol Plant 45:157–159

    Article  CAS  Google Scholar 

  • Gallo RL, Kochevar IE, Granstein RD (1989) 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

    Article  CAS  Google Scholar 

  • Gómez I, Figueroa FL, Sousa-Pinto I, Viñegla B, Pérez-Rodríguez E, Maestre C, Coelho S, Felga A, Pereira P (2001) Effects of UV radiation and temperature in hotosynthesis as mesured by PAM Fluorescence in red alga Gelidium pulchellum (Turner). Bot Mar 44:9-16

    Google Scholar 

  • Grossman AR, Schaefer MR, Chiang GG, Collier JL (1993) The phycobilisome a light harvesting complex responsive to environmental conditions. Microbiol Rev 57:725–749

    PubMed  CAS  Google Scholar 

  • Hideg E, Vass I (1996) UV-B induced free radical production in plant leaves and isolated thylakoid membranes. Plant Sci 115:251–260

    Article  CAS  Google Scholar 

  • Hiscox JD, Israelstam GF (1979) A method for the extraction of chlorophyll from leaf tissue without maceration. Can J Bot 57:1332–1334

    Article  CAS  Google Scholar 

  • 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 6:568–577

    Article  PubMed  CAS  Google 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 45:168–177

    Article  Google Scholar 

  • Holzinger A, Roleda MY, Lütz C (2009) The vegetative arctic freshwater green alga Zygnema is insensitive to experimental UV exposure. Micron 40:831–838

    Article  PubMed  Google Scholar 

  • Hulshof PJM, Kosmeijer-Schuil T, West CE, Hollman PCH (2007) Quick screening of maize kernels for provitamin A content. J Food Compos Anal 20:655–661

    Article  CAS  Google Scholar 

  • Iwanzik W, Tevini M, Dohnt G, Voss M, Weiss W, Gräber P, Renger G (1983) Action of UV-B radiation on photosynthetic primary reactions in spinach chloroplasts. Physiol Plant 58:401–407

    Article  CAS  Google 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 155:407–415

    Article  CAS  Google Scholar 

  • Kerr JB, Mc Elroy CT (1993) Evidence for large upward trends of ultraviolet-B radiation linked to ozone depletion. Science 262:1032–1034

    Article  PubMed  CAS  Google Scholar 

  • Kuhnen S, Lemos PMM, Campestrini LH, Ogliari JB, Dias PF, Maraschin M (2009) Antiangiogenic properties of carotenoids: a potential role of maize as functional food. J Funct Foods 1:284–290

    Article  CAS  Google Scholar 

  • Kursar TA, van Der Meer J, Alberte RS (1983) Light-harvesting system of the red alga Gracilaria tikvahiae. I. Biochemical analyses of pigment mutations. Plant Physiol 73:353–360

    Article  PubMed  CAS  Google Scholar 

  • Latini A, Rodriguez M, Borba RR, Scussiato K, Leipnitz G, Reis de Assis D, da Costa FG, Funchal C, Jacques-Silva MC, Buzin L, Giugliani R, Cassina A, Radi R, Wajner M (2005) 3-Hydroxyglutaric acid moderately impairs energy metabolism in brain of young rats. Neuroscience 135:111–120

    Article  PubMed  CAS  Google Scholar 

  • Lesser MP, Shick JM (1994) 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

    Article  Google Scholar 

  • Lowry OH, Rosebough NG, Farr AL (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193:265–275

    PubMed  CAS  Google Scholar 

  • Madronich S (1992) Implications of recent total atmospheric ozone measurements for biological active ultraviolet radiation reaching the Earths surface. Geophys Res Letters 19:37–40

    Article  CAS  Google Scholar 

  • Mitchell DL, Jen J, Cleaver JE (1992) Sequence specificity of cyclobutane pyrimidine dimers in DNA treated with solar (ultraviolet B) radiation. Nucleic Acids Res 20:225–229

    Article  PubMed  CAS  Google Scholar 

  • Murphy TM (1983) Membranes as targets of ultraviolet radiation. Physiol Plant 58:381–388

    Article  CAS  Google Scholar 

  • Neale PJ, Cullen JC, Lesser MP, Melis A (1993) Physiological bases for detecting and predicting photoinhibition of aquatic photosyn- thesis by PAR and UV radiation. In: Yamamoto HY, Smith CM (eds) Photosynthetic responses to the environment. Amer Soc Plant Physiol, Rockville, pp 61–77

  • 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. Mar Ecol Prog Ser 157:139–146

    Article  CAS  Google Scholar 

  • Penniman CA, Mathieson AC, Penniman CE (1986) Reproductive phenology and growth of Gracilaria tikvahiae McLachlan (Gigartinales, Rhodophyta) in the Great Bay Estuary, New Hampshire. Bot Mar 29:147–154

    Article  Google Scholar 

  • Platt T, Gallegos CL, Harrison WG (1980) Photoinhibition of photosynthesis in natural assemblages of marine phytoplankton. J Mar Res 38:687–701

    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 

  • Poppe F, Schmidt RAM, Hanelt D, Wiencke C (2003) Effects of UV radiation on the ultrastructure of several red algae. Phycol Res 51:11–19

    Google Scholar 

  • Post A, Gentle S, Larkum AWS (1992) Algal photosynthesis: inhibition by UV-B radiation, recovery and UV-absorbing pigments. In: Murata N (ed) Research in photosynthesis. Kluwer Academic, Dordrecht, pp 847–850

  • Roleda MY, van de Poll WH, 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. Mar Ecol Prog Ser 281:37–50

    Article  Google Scholar 

  • Roleda MY, 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 243:105–116

    Article  PubMed  Google Scholar 

  • Ruhland CT, Fogal MJ, Buyarski CR, Krna MA (2007) Solar ultraviolet-B radiation increases phenolic content and ferric reducing antioxidant power in Avena sativa. Molecules 12:1220–1232

    Article  PubMed  CAS  Google Scholar 

  • Schmidt EC, Scariot LA, Rover T, Bouzon ZL (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 40:860–869

    Article  PubMed  CAS  Google Scholar 

  • Schmidt EC, Maraschin M, Bouzon ZL (2010a) Effects of UVB radiation on the carragenophyte Kappaphycus alvarezii (Rhodophyta, Gigartinales): changes in ultrastructure, growth, and photosynthetic pigments. Hydrobiologia 649:171–182

    Article  CAS  Google Scholar 

  • Schmidt EC, Nunes BG, Maraschin M, Bouzon ZL (2010b) Effect of ultraviolet-B radiation on growth, photosynthetic pigments, and cell biology of Kappaphycus alvarezii (Rhodophyta, Gigartinales) macroalgae brown strain. Photosynthetica 48:161–172

    Article  CAS  Google Scholar 

  • Schmidt EC, Santos R, Horta P, Maraschin M, Bouzon ZL (2010c) Effects of UVB radiation on the agarophyte Gracilaria domingensis (Rhodophyta, Gracilariales): changes in cell organization, growth and photosynthetic performance. Micron 41:919–930

    Article  PubMed  CAS  Google Scholar 

  • Schmidt EC, Pereira B, Mansur-Lessa C, Santos R, Scherner F, Horta PA, Martins RP, Latini A, Maraschin M, Bouzon ZL (2011) Alterations in architecture and metabolism induced by ultraviolet radiation-B in the carragenophyte Chondracanthus teedei (Rhodophyta, Gigartinales). Protoplasma. doi:10.1007/s00709-011-0286-1

  • Scott CE, Eldridge AL (2005) Comparison of carotenoid content in fresh, frozen and, canned corn. J Food Comp Anal 18:551–559

    Article  CAS  Google Scholar 

  • Shiu CT, Lee TM (2005) Ultraviolet-B-induced oxidative stress and responses of the ascorbate-glutathione cycle in a marine macroalga Ulva fasciata. J Exper Bot 56:2851–2865

    Article  CAS  Google Scholar 

  • Sousa-Pinto I, Murano E, Coelho S, Felga A, Pereira R (1999) The effect of light on growth and agar content of Gelidium pulchellum (Gelidiaceae, Rhodophyta) in cultura. Hydrobiologia 398/399:329–338

    Article  CAS  Google Scholar 

  • Steinhoff FS, Wiencke C, Muller R, Bischof K (2008) Effects of ultraviolet radiation and temperature on the ultrastructure of zoospores of the brown macroalga Laminaria hyperborean. Plant Biology 10:388–397

    Google Scholar 

  • Strid A, Chow WS, Anderson JM (1994) UV-B damage and protection at the molecular level in plants. Photosynth Res 39:475–489

    Article  CAS  Google Scholar 

  • Talarico L (1996) Phycobiliproteins and phycobilisomes in red algae: adaptive responses to light. Sci Mar 60:205–222

    CAS  Google Scholar 

  • van de Poll WH, Eggert A, Buma GJ, 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 37:30–38

    Article  Google Scholar 

  • Vass I (1997) Adverse effects of UV-B light on the structure and function of the photosynthetic apparatus. In: Pessarakali M (ed) Handbook of photosynthesis. Marcel Dekker, New York

  • Wellburn AR (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 144:307–313

    Article  CAS  Google Scholar 

  • White AK, Critchley C (1999) Rapid light curves: a new fluorescence method to assess the state of the photosynthetic apparatus. Photosynth Res 59:63–72

    Article  CAS  Google Scholar 

  • Wood WF (1989) Photoadaptive responses of the tropical red alga Eucheuma striatum Schmitz (Gigartinales) to ultra-violet radiation. Aquat Bot 33:41–51

    Article  Google Scholar 

  • Xu J, Gao K (2007) Growth, pigments, UV-absorbing compounds and agar yield of the economic red seaweed Gracilaria lemaneiformis (Rhodophyta) grown at different depths in the coastal waters of the South China Sea. J Appl Phycol 20:681–686

    Article  Google Scholar 

  • Yakovleva IM, Titlyanov EA (2001) Effect of high visible and UV irradiance on subtidal Chondrus crispus: stress, photoinhibition and protective mechanism. Aquat Bot 71:47–61

    Article  CAS  Google Scholar 

  • Yokoya NS, Necchi O Jr, Martins AP, Gonzalez SF, Plastino EM (2007) Growth responses and photosynthetic characteristics of wild and phycoerythrin-deficient strains of Hypnea musciformis (Rhodophyta). J App Phycol 19:197–205

    Article  CAS  Google Scholar 

Download references

Acknowledgments

The authors would like to acknowledge the staff of the Central Laboratory of Electron Microscopy (LCME), Federal University of Santa Catarina, Florianopolis, Santa Catarina, Brazil, for the use of their transmission electron microscope. This study was supported in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES, Brazil) and Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq, Brazil). The authors are grateful to CAPES for providing a scholarship to Éder C. Schmidt, Bouzon ZL, Maraschin M, Horta P.A, and Latini A are CNPq fellows. This study is part of the Ph.D. thesis of the first author.

Conflict of interest

The authors declare that they have no conflict of interest.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Éder C. Schmidt.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Schmidt, É.C., dos Santos, R.W., de 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). https://doi.org/10.1007/s10811-012-9786-4

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10811-012-9786-4

Keywords

Navigation