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Effects of cadmium on the morphology, pigments, and ultrastructure of Palisada flagellifera (Ceramiales, Rhodophyta) cultivated in vitro

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Abstract

This study aimed to compare the effects of increasing concentrations of cadmium (Cd) on the growth rates, content of photosynthetic pigments, and ultrastructure of Palisada flagellifera (J. Agardh) K. W. Nam (Ceramiales, Rhodophyta). Plants were cultivated under photosynthetically active radiation (PAR) of 70 μmol photons m−2 s−1 with 0 (control), 2.5, 5.0, 7.5, 10 20, 40, and 60 μM of cadmium (CdCl2) for 7 days. Subsequently, the apical segments of P. flagellifera were analyzed under transmission microscopy, and both growth rates and photosynthetic pigments were measured. Growth rates in P. flagellifera samples gradually decreased with the increasing concentration of Cd in culture medium. Palisada flagellifera exposed to 20, 40, and 60 μM of Cd showed thallus bleaching and partial necrosis. Damage to thylakoid membranes and discoloration, as well as reduced phycobiliproteins, were more evident at concentrations of Cd higher than 40 µM. Palisada flagellifera samples treated with Cd also showed cell wall thickness triggered by the activation of mechanical defense mechanisms to prevent entry of Cd into the cytoplasm, as well as the increase of chlorophyll a content. Overall, these results indicate that exposure to cadmium in concentrations exceeding 40 µM is sublethal to P. flagellifera.

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References

  • Andrade LR, Farina M, Amado Filho GM (2002) Role of Padina gymnospora (Dictyotales, Phaeophyceae) cell walls in cadmium accumulation. Phycologia 41:39–48

    Article  Google Scholar 

  • Bouzon ZL, Ferreira EC, Santos R, Scherner F, Horta PA, Maraschin M, Schmidt EC (2012) Influences of cadmium on fine structure and metabolism of Hypnea musciformis Rhodophyta, Gigartinales cultivated in vitro. Protoplasma 249:637–650

    Article  CAS  PubMed  Google Scholar 

  • Brito NRB (2011). Efeito de metais pesados na alga Pseudokirchneriella subcapitata. Dissertação de Mestrado, Instituto Superior de Engenharia do Porto, Porto

  • Cassano V (2009) Taxonomia e Filogenia do complexo Laurencia (Ceramiales, Rhodophyta), com ênfase no estado do Rio de Janeiro. Tese de Doutorado, Instituto de Botânica de São Paulo, São Paulo

    Google Scholar 

  • Collén J, Pinto E, Pedersén M, Colepicolo P (2003) Induction of oxidative stress in the red macroalgae Gracilaria tenuisitipitata by pollutant metals. Arch Environ Contam Toxicol 45:337–342

    Article  PubMed  Google Scholar 

  • de Felix MR, Osorio LKP, Ouriques LC, Farias-Soares FL, Steiner N, Kreusch M, Pereira DT, Simioni C, Costa GB, Horta PA, Chow F, Ramlov F, Maraschin M, Bouzon ZL, Schmidt EC (2014) 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

    Article  Google Scholar 

  • Diannelidis BE, Delivopoulos SG (1997) The effects of zinc, copper and cadmium on the fine structure of Ceramium ciliatum (Rhodophyceae, Ceramiales). Mar Environ Res 44:127–134

    Article  CAS  Google Scholar 

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

    Google Scholar 

  • Esteban R, Martínez B, Fernández-Marín B, Jm Becerril, García-Plazaola JI (2009) Carotenoid composition in Rhodophyta: insights into xanthophyll regulation in Corallina elongata. Eur J Phycol 44:221–230

    Article  CAS  Google Scholar 

  • Gil-Rodríguez MC, Cassano V, Aylagas E, Sentíes A, Díaz-Larrea J, Oliveira MC, Fujii MT (2010) Palisada flagellifera (Ceramiales, Rhodophyta) from the Canary Islands, Spain: a new record for the eastern Atlantic Ocean based on morphological and molecular evidence. Bot Mar 53:31–40

    Article  Google Scholar 

  • Gouveia C, Kreusch M, Schmidt EC, Felix MRL, Osorio LKP, Pereira DT, Santos R, Ouriques LC, Martins RP, Latini A, Ramlov F, Carvalho TJG, Chow F, Maraschin M, Bouzon ZL (2013) The effects of lead and copper on the cellular architecture and metabolism of the red alga Gracilaria domingensis. Microsc Microanal 19:513–524

    Article  CAS  PubMed  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 

  • Kumar S, Roop NG (2012) Regulation for safety and quality of cosmetics vis-a-vis colourants in India compared with other nations. Der Pharmacia Lettre 1:181–191

    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  CAS  PubMed  PubMed Central  Google Scholar 

  • Lignell A, Pedersén M (1989) Agar composition as a function of morphology and growth rate. Studies on some morphological strains of Gracilaria secundata and Gracilaria verrucosa (Rhodophyta). Bot Mar 32:219–227

    Article  CAS  Google Scholar 

  • Loitzenbauer E, Mendes CAB (2014) The terrestrial coastal zone and the water resources in the South Atlantic Hydrographical Region, Brazil. Coastal Zone Manag 14:81–94

    Google Scholar 

  • Mamboya FA, Pratap HB, Mtolera M, Bjork M (1999) The effect of copper on the daily growth rate and photosynthetic efficiency of the brown macroalga Padina boergensenii. In: Richmond MD, Francis J (eds) Proceedings of the conference on advances on marine sciences in Tanzania, pp 185-192

  • Ouriques LC, Schmidt EC, Bouzon ZL (2012) The mechanism of adhesion and germination in the carpospores of Porphyra spiralis var. amplifolia (Rhodophyta, Bangiales). Micron 43:269–277

    Article  CAS  PubMed  Google Scholar 

  • Pinto E, Sigaud-Kutner TCS, Leitão MAS, Okamoto OK, Morse D, Colepicolo P (2003) Heavy metal-induced oxidative stress in algae. J Phycol 39:1008–1018

    Article  CAS  Google Scholar 

  • Reynolds ES (1963) The use of lead citrate at light pH as an electron opaque stain in electron microscopy. J Cell Biol 17:208–212

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Santos R, Schmidt EC, Paula MR, Latini A, Horta PA, Maraschin M, Bouzon ZL (2012) Effects of cadmium on growth, photosynthetic pigments, photosynthetic performance, biochemical parameters and structure of chloroplasts in the agarophyte Gracilaria domingensis (Rhodophyta, Gracilariales). Am J Plant Sci 3:1077–1084

    Article  Google Scholar 

  • Santos RW, Schmid EC, Bouzon ZL (2013) Changes in ultrastructure and cytochemistry of the agarophyte Gracilaria domingensis (Rhodophyta, Gracilariales) treated with cadmium. Protoplasma 250:297–305

    Article  CAS  PubMed  Google Scholar 

  • Santos RW, Schmidt EC, Felix MR, Polo LK, Kreusch M, Pereira DT, Costa GB, Simioni C, Chowd F, Ramlov F, Maraschin M, Bouzon ZL (2014) Bioabsorption of cadmium, copper and lead by the red macroalga Gelidium floridanum: physiological responses and ultrastructure features. Ecotox Environ Safe 105:80–89

    Article  Google Scholar 

  • Scandalios JG (1993) Regulation and properties of plant catalases. In: Foyer CH, Mullineaux PM (eds) Causes of photooxidative stress and amelioration of defense systems in plants. CRC Press, Boca Raton, pp 275–315

    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  CAS  PubMed  Google Scholar 

  • Schmidt EC, Pereira B, Pontes CLM, Santos R, Scherner F, Horta PA, Paula MR, Latini A, Maraschin M, Bouzon ZL (2012) Alterations in architecture and metabolism induced by ultraviolet radiation-B in the carragenophyte Chondracanthus teedei (Rhodophyta, Gigartinales). Protoplasma 249:353–367

    Article  CAS  PubMed  Google Scholar 

  • Schmidt EC, Kreusch M, Felix M, Pereira D, Costa G, Simioni C, Ouriques L, Farias-Soares F, Steiner N, Chow F, Ramlov F, Maraschin M, Bouzon ZL (2015) Effects of ultraviolet radiation (UVA+UVB) and copper on the morphology, ultrastructural organization and physiological responses of the red alga Pterocladiella capillacea. Photochem Photobiol 91:359–370

    Article  CAS  PubMed  Google Scholar 

  • Silva DMS (2010). Estudo do processo adsortivo de cádmio por Algas Arribadas. Dissertação de Mestrado, Universidade Federal de Pernambuco, Recife

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

    CAS  Google Scholar 

  • Talarico L (2002) Fine structure and X-ray microanalysis of a red macrophyte cultured under cadmium stress. Environ Pollut 120:813–821

    Article  CAS  PubMed  Google Scholar 

  • Visvik I, Rachlin JW (1992) Ultrastructural changes in Dunaliella minuta following acute and chronic exposure to copper and cadmium. Arch Environ Contam Toxicol 23:420–425

    Google Scholar 

  • 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 

  • Xia JR, Li YJ, Lu J, Chen B (2004) Effects of copper and cadmium on growth, photosynthesis and pigment content in Gracilaria lemaneiformis. Bull Environ Contam Toxicol 73:979–986

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

The authors would like to thank the staff of the Central Laboratory of Electron Microscopy (LCME), the Federal University of Santa Catarina, Florianopolis, Santa Catarina, Brazil, for allowing the use of their scanning and transmission electron microscopes.

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Authors and Affiliations

  1. Plant Cell Biology Laboratory, Department of Cell Biology, Embryology and Genetics, Federal University of Santa Catarina, CP 476, Florianópolis, SC, 88049-900, Brazil

    Brunna Simonetti, Éder C. Schmidt, Débora T. Pereira, Zenilda L. Bouzon & Luciane C. Ouriques

  2. Postdoctoral Research of Postgraduate Program in Cell Biology and Development, Department of Cell Biology, Embryology and Genetics, Federal University of Santa Catarina, CP 476, Florianópolis, SC, 88049-900, Brazil

    Éder C. Schmidt

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  1. Brunna Simonetti
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  2. Éder C. Schmidt
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  5. Luciane C. Ouriques
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Correspondence to Éder C. Schmidt.

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Simonetti, B., Schmidt, É.C., Pereira, D.T. et al. Effects of cadmium on the morphology, pigments, and ultrastructure of Palisada flagellifera (Ceramiales, Rhodophyta) cultivated in vitro. Braz. J. Bot 39, 465–473 (2016). https://doi.org/10.1007/s40415-016-0254-2

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  • DOI: https://doi.org/10.1007/s40415-016-0254-2

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