JOURNAL BROWSE
Search
Advanced SearchSearch Tips
Chloroplasts morphology investigation with diverse microscopy approaches and inter-specific variation in Laurencia species (Rhodophyta)
facebook(new window)  Pirnt(new window) E-mail(new window) Excel Download
  • Journal title : ALGAE
  • Volume 30, Issue 4,  2015, pp.291-301
  • Publisher : The Korean Society of Phycology
  • DOI : 10.4490/algae.2015.30.4.291
 Title & Authors
Chloroplasts morphology investigation with diverse microscopy approaches and inter-specific variation in Laurencia species (Rhodophyta)
Paradas, Wladimir Costa; Andrade, Leonardo Rodrigues; Salgado, Leonardo Tavares; Collado-Vides, Ligia; Pereira, Renato Crespo; Amado-Filho, Gilberto Menezes;
  PDF(new window)
 Abstract
The present study described with different microscopy approaches chloroplasts lobes in Laurencia sensu latu (Rhodophyta) species and found inter-specific differences among them. Chloroplasts were investigated using confocal laser scanning microscopy (LSM), transmission electron microscopy (TEM) and high resolution scanning electron microscopy (HRSEM). Using and TEM and HRSEM images we distinguished chloroplasts with lobes than chloroplasts without lobes in Yuzurua poiteaui var. gemmifera (Harvey) M. J. Wynne and Laurencia dendroidea J. Agardh cortical cells. The LSM images showed chloroplasts lobes (CLs) with different morphologies, varying from thicker and longer undulated projections in Y. poiteaui var. and L. dendroidea to very small and thin tubules as in Laurencia translucida Fujii & Cordeiro-Marino. The diameter and length of CLs from Y. poiteaui var. and L. dendroidea were significantly higher than L. translucida CLs (p < 0.01). Based on LSM observations, we suggest that lobes morphology has a taxonomic validity only to characterize L. translucida species.
 Keywords
chloroplasts lobes;confocal laser scanning microscopy;Laurencia dendroidea;Laurencia translucida;morphometry;transmission electron microscopy;Yuzurua poiteaui var. gemmifera;
 Language
English
 Cited by
 References
1.
Abe, T., Kurihara, A., Kawaguchi, S., Terada, R. & Masuda, M. 2006. Preliminary report on the molecular phylogeny of the Laurencia complex (Rhodomelaceae). Coast. Mar. Sci. 30:209-213.

2.
Abramoff, M. D., Magalhães, P. J. & Ram, S. J. 2004. Image processing with ImageJ. Biophotonics Int. 11:36-42.

3.
Barnabas, A. D. 1982. Fine structure of the leaf epidermis of Thalassodendron ciliatum (Forsk.) den Hartog. Aquat. Bot. 12:41-55. crossref(new window)

4.
Bisalputra, T. & Bailey, A. 1973. The fine structure of the chloroplast envelope of a red alga, Bangia fusco-purpurea. Protoplasma 76:443-454. crossref(new window)

5.
Bouzon, Z. L., Chow, F., Zitta, C. S., Dos Santos, R. W., Ouriques, L. C., Felix, M. R. L., Osorio, L. K. P., Gouveia, C., Martins, R. P., Latini, A., Ramlov, F., Maraschin, M. & Schmidt, E. C. 2012. 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). Microsc. Microanal. 18:1467-1479. crossref(new window)

6.
Cole, K. & Sheath, R. G. 1980. Ultrastructural changes in major organelles during spermatial differentiation in Bangia (Rhodophyta). Protoplasma 102:253-279. crossref(new window)

7.
Crews, P. & Selover, S. J. 1986. Comparison of the sesquiterpenes from the seaweed Laurencia pacifica and its epiphyte Erythrocystis saccata. Phytochemistry 25:1847-1852. crossref(new window)

8.
Da Gama, B. A. P., Pereira, R. C., Soares, A. R., Teixeira, V. L. & Yoneshigue-Valentin, Y. 2003. Is the mussel test a good indicator of antifouling activity? A comparison between laboratory and field assays. Biofouling 19:161-169. crossref(new window)

9.
Da Gama, B. A. P., Plouguerné, E. & Pereira, R. C. 2014. The antifouling defence mechanisms of marine macroalgae. In Bourgougnon, N. (Ed.) Advances in Botanical Research. Elsevier B.V., Amsterdam, pp. 413-440.

10.
De Oliveira, L. S., Gregoracci, G. B., Silva, G. G. Z., Salgado, L. T., Filho, G. A., Alves-Ferreira, M., Pereira, R. C. & Thompson, F. L. 2012. Transcriptomic analysis of the red seaweed Laurencia dendroidea (Florideophyceae, Rhodophyta) and its microbiome. BMC Genomics 13:487. crossref(new window)

11.
De Oliveira, L. S., Tschoeke, D. A., De Oliveira, A. S., Hill, L. J., Paradas, W. C., Salgado, L. T., Thompson, C. C., Pereira, R. C. & Thompson, F. L. 2015. New insights on the terpenome of the red seaweed Laurencia dendroidea (Florideophyceae, Rhodophyta). Mar. Drugs 13:879-902. crossref(new window)

12.
Díaz-Larrea, J., Sentíes, A., Fujii, M. T., Pedroche, F. F. & Oliveira, M. C. 2007. Molecular evidence for Chondrophycus poiteaui var. gemmiferus comb. et stat. nov. (Ceramiales, Rhodophyta) from the Mexican Caribbean Sea: implications for the taxonomy of the Laurencia complex. Bot. Mar. 50:250-256.

13.
Dos Santos, R. W., Schmidt, E. C., Felix, M. R. L., Polo, L. K., Kreusch, M., Pereira, D. T., Costa, G. B., Simioni, C., Chow, F., Ramlov, F., Maraschin, M. & Bouzon, Z. L. 2014. Bioabsorption of cadmium, copper and lead by the red macroalga Gelidium floridanum: physiological responses and ultrastructure features. Ecotoxicol. Environ. Saf. 105:80-89. crossref(new window)

14.
Feldmann, J. & Feldmann, G. 1950. Les “corps en cerise” des Laurencia (Rhodomelacées, Ceramiales). C. R. Acad. Sci. Paris Ser. D 266:2393-2396.

15.
Fujii, M. T., Cassano, V., Stein, E. M. & Carvalho, L. R. 2011. Overview of the taxonomy and of the major secondary metabolites and their biological activities related to human health of the Laurencia complex (Ceramiales, Rhodophyta) from Brazil. Braz. J. Pharmacogn. 21:268-282.

16.
Fujii, M. T., Guimarães, S. M. P. B., Gurgel, C. F. D. & Fredericq, S. 2006. Characterization and phylogenetic affinities of the red alga Chondrophycus flagelliferus (Rhodomelaceae, Ceramiales) from Brazil on the basis of morphological and molecular evidence. Phycologia 45:432-441. crossref(new window)

17.
Garbary, D. J. & Gabrielson, P. W. 1990. Taxonomy and evolution. In Cole, K. M. & Sheath, R. G. (Eds.) Biology of the Red Algae. Cambridge University Press, Cambridge, pp. 477-498.

18.
Garbary, D. J. & Harper, J. T. 1998. A phylogenetic analysis of the Laurencia complex (Rhodomelaceae) of the red algae. Cryptogam. Algol. 19:185-200.

19.
Geitler, L. 1927. Rhodospora sordida, nov. gen. et n. sp., eine neue ‘Bangiacee’ des Süßwassers. österr. Bot. Z. 76:25-28. crossref(new window)

20.
Gillard, J., Devos, V., Huysman, M. J. J., De Veylder, L., D’Hondt, S., Martens, C., Vanormelingen, P., Vannerum, K., Sabbe, K., Chepurnov, V. A., Inz&é, D., Vuylsteke, M. & Vyverman, W. 2008. Physiological and transcriptomic evidence for a close coupling between chloroplast ontogeny and cell cycle progression in the pennate diatom Seminavis robusta. Plant Physiol. 148:1394-1411. crossref(new window)

21.
Gil-Rodríguez, M. C., Sentíes, A., Díaz-Larrea, J., Cassano, V. & Fujii, M. T. 2009. Laurencia marilzae sp. nov. (Ceramiales, Rhodophyta) from the Canary Islands, Spain, based on morphological and molecular evidence. J. Phycol. 45:264-271. crossref(new window)

22.
Gouveia, C., Kreusch, M., Schmidt, E. C., Felix, M. R. L., Osorio, L. K. P., Pereira, D. T., Dos Santos, R., Ouriques, L. C., Martins, R. P., Latini, A., Ramlov, F., Carvalho, T. J. G., Chow, F., Maraschin, M. & Bouzon, Z. L. 2013. The effects of lead and copper on the cellular architecture and metabolism of the red alga Gracilaria domingensis. Microsc. Microanal. 19:513-524. crossref(new window)

23.
Hanson, M. R. & Sattarzadeh, A. 2011. Stromules: recent insights into a long neglected feature of plastid morphology and function. Plant Physiol. 155:1486-1492. crossref(new window)

24.
Johansen, J. R., Fučíková, K., Fitzpatrick, M. H. & Lowe, R. L. 2005. The red alga genus Rhodospora (Bangiophyceae, Rhodophyta): first report from North America. J. Phycol. 41:1281-1283. crossref(new window)

25.
Kachar, B., Parakkal, M., Kurc, M., Zhao, Y. & Gillespie, P. G. 2000. High-resolution structure of hair-cell tip links. Proc. Natl. Acad. Sci. U. S. A. 97:13336-13341. crossref(new window)

26.
Kachar, B. & Reese, T. S. 1988. The mechanism of cytoplasmic streaming in characean algal cells: sliding of endoplasmic reticulum along actin filaments. J. Cell Biol. 106:1545-1552. crossref(new window)

27.
Kikuchi, N. & Shin, J. -A. 2005. Morphology and life history of Stylonema cornu-cervi Reinsch (Goniotrichales, Rhodophyta) from Japan. Algae 20:37-42. crossref(new window)

28.
Kushibiki, A., Yokoyama, A., Iwataki, M., Yokoyama, J., West, J. A. & Hara, Y. 2012. New unicellular red alga, Bulboplastis apyrenoidosa gen. et sp. nov. (Rhodellophyceae, Rhodophyta) from the mangroves of Japan: phylogenetic and ultrastructural observations. Phycol. Res. 60:114-122. crossref(new window)

29.
Martin-Lescanne, J., Rousseau, F., De Reviers, B., Payri, C., Couloux, A., Cruaud, C. & Le Gall, L. 2010. Phylogenetic analyses of the Laurencia complex (Rhodomelaceae, Ceramiales) support recognition of five genera: Chondrophycus, Laurencia, Osmundea, Palisada and Yuzurua stat. nov. Eur. J. Phycol. 45:51-61. crossref(new window)

30.
Menzel, D. 1994. An interconnected plastidom in Acetabularia: implications for the mechanism of chloroplast motility. Protoplasma 179:166-171. crossref(new window)

31.
Metti, Y., Millar, A. J. K. & Steinberg, P. 2015. A new molecular phylogeny of the Laurencia complex (Rhodophyta, Rhodomelaceae) and a review of key morphological characters result in a new genus, Coronaphycus, and a description of C. novus. J. Phycol. 51:929-942. crossref(new window)

32.
Müller, K. M., Lynch, M. D. J. & Sheath, R. G. 2010. Bangiophytes: from one class to six; where do we go from here? In Seckbach, J. & Chapman, D. J. (Eds.) Red Algae in the Genomic Age, Cellular Origin, Life in Extreme Habitats and Astrobiology. Springer-Verlag, Berlin, pp. 241-259.

33.
Nam, K. W. 1999. Morphology of Chondrophycus undulate and C. parvipapillata and its implications for the taxonomy of the Laurencia (Ceramiales, Rhodophyta) complex. Eur. J. Phycol. 34:455-468. crossref(new window)

34.
Nam, K. W. 2006. Phylogenetic re-evaluation of the Laurencia complex (Rhodophyta) with a description of L. succulenta sp. nov. from Korea. J. Appl. Phycol. 18:679-697. crossref(new window)

35.
Nam, K. W., Maggs, C. A. & Garbary, D. J. 1994. Resurrection of the genus Osmundea with an emendation of the generic delineation of Laurencia (Ceramiales, Rhodophyta). Phycologia 33:384-395. crossref(new window)

36.
Nam, K. W., Maggs, C. A., McIvor, L. & Stanhope, M. J. 2000. Taxonomy and phylogeny of Osmundea (Rhodomelaceae, Rhodophyta) in Atlantic Europe. J. Phycol. 36:759-772. crossref(new window)

37.
Natesan, S. K. A., Sullivan, J. A. & Gray, J. C. 2005. Stromules: a characteristic cell-specific feature of plastid morphology. J. Exp. Bot. 56:787-797 crossref(new window)

38.
Paradas, W. C. 2013. Mecanismos de armazenamento, biossíntese e liberação de metabólitos secundários em macroalgas vermelhas (Rhodophyta) in Brazil. Ph.D. dissertation, Universidade Federal Fluminense, Niterói, Brazil, 179 pp.

39.
Paradas, W. C., Crespo, T. M., Salgado, L. T., De Andrade, L. R., Soares, A. R., Hellio, C., Paranhos, R. R., Hill, L. J., De Souza, G. M., Kelecom, A. G. A. C., Da Gama, B. A. P., Pereira, R. C. & Amado-Filho, G. M. 2015. Mevalonosomes: specific vacuoles containing the mevalonate pathway in Plocamium brasiliense cortical cells (Rhodophyta). J. Phycol. 51:225-235. crossref(new window)

40.
Paradas, W. C., Salgado, L. T., Sudatti, D. B., Crapez, M. A., Fujii, M. T., Coutinho, R., Pereira, R. C. & Amado Filho, G. M. 2010. Induction of halogenated vesicle transport in cells of the red seaweed Laurencia obtusa. Biofouling 26:277-286. crossref(new window)

41.
Proctor, M. C. F., Ligrone, R. & Duckett, J. G. 2007. Desiccation tolerance in the moss Polytrichum formosum: physiological and fine-structural changes during desiccation and recovery. Ann. Bot. 99:75-93. crossref(new window)

42.
Pyke, K. A. & Page, A. M. 1998. Plastid ontogeny during petal development in Arabidopsis. Plant Physiol. 116:797-803. crossref(new window)

43.
Reis, V. M., Oliveira, L. S., Passos, R. M. F., Viana, N. B., Mermelstein, C., Sant’Anna, C., Pereira, R. C., Paradas, W. C., Thompson, F. L., Amado-Filho, G. M. & Salgado, L. T. 2013. Traffic of secondary metabolites to cell surface in the red alga Laurencia dendroidea depends on a two-step transport by the cytoskeleton. PLoS ONE 8:e63929. crossref(new window)

44.
Saito, Y. 1967. Studies on Japanese species of Laurencia, with special reference to their comparative morphology. Mem. Fac. Fish. Hokkaido Univ. 15:1-81.

45.
Salgado, L. T., Viana, N. B., Andrade, L. R., Leal, R. N., Da Gama, B. A. P., Attias, M., Pereira, R. C. & Amado Filho, G. M. 2008. Intra-cellular storage, transport and exocytosis of halogenated compounds in marine red alga Laurencia obtusa. J. Struct. Biol. 162:345-355. crossref(new window)

46.
Sarafis, V. 1998. Chloroplasts: a structural approach. J. Plant Physiol. 152:248-264. crossref(new window)

47.
Schmidt, E. C., Pereira, B., Dos Santos, R. W., Gouveia, C., Costa, G. B., Faria, G. S. M., Scherner, F., Horta, P. A., Martins, R. P., Latini, A., Ramlov, F., Maraschin, M. & Bouzon, Z. L. 2012. Responses of the macroalgae Hypnea musciformis after in vitro exposure to UV-B. Aquat. Bot. 100:8-17. crossref(new window)

48.
Schottkowski, M., Peters, M., Zhan, Y., Rifai, O., Zhang, Y. & Zerges, W. 2012. Biogenic membranes of the chloroplast in Chlamydomonas reinhardtii. Proc. Natl. Acad. Sci. U. S. A. 109:19286-19291. crossref(new window)

49.
Škaloud, P., Neustupa, J., Radochová, B. & Kubínová, L. 2005. Confocal microscopy of chloroplast morphology and ontogeny in three strains of Dictyochloropsis (Trebouxiophyceae, Chlorophyta). Phycologia 44:261-269. crossref(new window)

50.
Sudatti, D. B., Rodrigues, S. V. & Pereira, R. C. 2006. Quantitative GC-ECD analysis of halogenated metabolites: determination of surface and within-thallus elatol of Laurencia obtusa. J. Chem. Ecol. 32:835-843. crossref(new window)

51.
Suzuki, M., Kurosawa, E. & Kurata, K. 1987. (E)-Tridecyl-2-heptadecenal, an unusual metabolites from the red alga Laurencia species. Bull. Chem. Soc. Jpn. 60:3793-3794. crossref(new window)

52.
Tischendorf, G., Oesterhelt, C., Hoffmann, S., Girnus, J., Schnarrenberger, C. & Gross, W. 2007. Ultrastructure and enzyme complement of proplastids from heterotrophically grown cells of the red alga Galdieria sulphuraria. Eur. J. Phycol. 42:243-251. crossref(new window)

53.
Wilson, S., West, J., Pickett-Heaps, J., Yokoyama, A. & Hara, Y. 2002. Chloroplast rotation and morphological plasticity of the unicellular alga Rhodosorus (Rhodophyta, Stylonematales). Phycol. Res. 50:183-191. crossref(new window)

54.
Yoon, H. S., Ciniglia, C., Wu, M., Comeron, J. M., Pinto, G., Pollio, A. & Bhattacharya, D. 2006. Establishment of endolithic populations of extremophilic Cyanidiales (Rhodophyta). BMC Evol. Biol. 6:78. crossref(new window)

55.
Young, D. N. 1978. Ultrastructural evidence for a secretory function in the “land cells” of the marine red alga Botryodadia pseudodichotoma (Rhodymeniaceae). Protoplasma 94:109-126. crossref(new window)

56.
Zheng, P., Wetzel, C., Ammar, K., Girard, A. -M. M., Rodermel, S., Thomas, D. R., Ning, L., Callis, J. B., Edwards, G. E. & Daley, L. 2002. Test of an in vivo method to detect chloroplast division in crop plants. Part II: verification of the phenomenon by germplasm methods and confocal microscopy. Spectroscopy 17:14-18.