Porphyra: Complex Life Histories in a Harsh Environment: P. umbilicalis, an Intertidal Red Alga for Genomic Analysis

  • Elisabeth Gantt
  • G. Mine Berg
  • Debashish Bhattacharya
  • Nicolas A. Blouin
  • Juliet A. Brodie
  • Cheong Xin Chan
  • Jonas Collén
  • Francis X. CunninghamJr
  • Jeferson Gross
  • Arthur R. Grossman
  • Steven Karpowicz
  • Yukihiro Kitade
  • Anita S. Klein
  • Ira A. Levine
  • Senjie Lin
  • Shan Lu
  • Michael Lynch
  • Subhash C. Minocha
  • Kirsten Müller
  • Christopher D. Neefus
  • Mariana Cabral de Oliveira
  • Linda Rymarquis
  • Alison Smith
  • John W. Stiller
  • Wen-Kai Wu
  • Charles Yarish
  • Yun Zhuang
  • Susan H. Brawley
Chapter
First Online:

Abstract

Porphyra encompasses a large group of multicellular red algae that have a prominent gametophytic phase. The complex, heteromorphic life history of species in this genus, their remarkable resilience to high light and desiccation, ancient fossil records, and value as human food (e.g., laver, nori), make Porphyra a compelling model for genome sequencing. Sequencing of the nuclear genome of Porphyra umbilicalis from the northwestern Atlantic is currently in process. The ∼270 Mb genome of this alga is much larger than that of the unicellular acidophilic Cyanidioschyzon merolae (16.5 Mb), the only rhodophyte for which there is a fully sequenced genome, and is approximately twice as large as the Arabidopsis genome. Future analyses of the P. umbilicalis genome should provide opportunities for researchers to (1) develop an increased understanding of the ways in which these algae have adapted to severe physiological stresses, (2) elucidate the molecular features of development through the complex life history, and (3) define key components required for the transition of growth from a single cell to a multicellular organism.

Keywords

Antioxidant aquaculture carotenoid cell motility cell walls chloroplast Cyanidioschyzon merolae genome evolution intertidal microRNAs mutants nitrogen sources nitrogen nori P. yezoensis P. umbilicalis Porphyra spores transposable elements vitamin B12 

References

  1. Ackland, J.C., West, J.A. and Pickett-Heaps, J. (2007) Actin and myosin regulate pseudopodia of Porphyra pulchella (Rhodophyta) archeospores. J. Phycol. 43: 129–138.CrossRefGoogle Scholar
  2. Algarra, P., Thomas, J.-C. and Mousseau, A. (1990) Phycobilisome heterogeneity in the red alga Porphyra umbilicalis. Plant Physiol. 92: 670–576.CrossRefGoogle Scholar
  3. Asamizu, E., Nakajima, M., Kitade, Y., Saga, N., Nakamura, Y. and Tabata, S. (2003) Comparison of RNA expression profiles between the two generations of Porphyra yezoensis (Rhodophyta), based on expressed sequence tag frequency analysis. J. Phycol. 39: 923–930.CrossRefGoogle Scholar
  4. Baldauf, S.L. (2008) An overview of the phylogeny and diversity of eukaryotes. J. Syst. Evol. 46: 263–273.Google Scholar
  5. Barbier, G., Oesterhelt, C., Larson, M.D., Halgren, R.G., Wilkerson, C., Garavito, R.M., Benning, C. and Weber, A.P.M. (2005) Comparative genomics of two closely related unicellular thermo-acidophilic red algae, Galdieria sulphuraria and Cyanidioschyzon merolae, reveals the molecular basis of the metabolic flexibility of Galdieria sulphuraria and significant differences in carbohydrate metabolism of both algae. Plant Physiol. 137: 460–474.PubMedCrossRefGoogle Scholar
  6. Bhattacharya, D., Cannone, J.J. and Gutell, R.R. (2001) Group I intron lateral transfer between red and brown algal ribosomal RNA. Curr. Genet. 40: 82–90.CrossRefGoogle Scholar
  7. Blouin, N., Fei, X.G., Peng, J., Yarish, C. and Brawley, S.H. (2007) Seeding nets with neutral spores of the red alga Porphyra umbilicalis (L.) Kützing for use in integrated multitrophic aquaculture (IMTA). Aquaculture. 270: 77–91.CrossRefGoogle Scholar
  8. Boucher, Y., Douady, C.J., Papke, R.T., Walsh, D.A., Boudreau, M.E.R., Nesbø, C.L., Case, R.J. and Doolittle, W.F. (2003) Lateral gene transfer and the origins of prokaryotic groups. Annu. Rev. Genet. 37: 283–328.PubMedCrossRefGoogle Scholar
  9. Bourne, V.L., Conway, E. and Cole, K. (1970) On the ultrastructure of pit connections in the Conchocelis phase of the red alga Porphyra perforata. Phycologia 9: 79–82.CrossRefGoogle Scholar
  10. Brodie, J. and Zuccarello, G.C. (2007) Systematics of the species-rich algae: red algal classification, phylogeny and speciation, In: R.T. Hodkinson, J. Parnell and S. Waldren (eds.) The Taxonomy and Systematics of Large and Species-Rich Taxa: Building and Using the Tree of Life. Systematics Association Series. CRC Press, Boca Raton, FL, pp. 317–330.Google Scholar
  11. Brodie, J. and Irvine, L.M. (2003) Seaweeds of the British Isles. Vol. 1 Part 3B. Bangiophycidae. Intercept, Hampshire.Google Scholar
  12. Brodie, J., Irvine, L., Neefus, C.D. and Russell, S. (2008) Ulva umbilicalis L. and Porphyra umbilicalis Kütz. (Rhodophyta, Bangiaceae): a molecular and morphological redescription of the species, with a typification updata. Taxon 57: 1328–1331.Google Scholar
  13. Butterfield, N.J. (2000) Bangiomorpha pubescens n. gen., n. sp.: implications for the evolution of sex, multicellularity and the Mesoproterozoic–Neoproterozoic radiation of eukaryotes. Paleobiology 26: 386–404.CrossRefGoogle Scholar
  14. Carmona, R., Kraemer, G.P. and Yarish, C. (2006) Exploring Northeast American and Asian species of Porphyra for use in an integrated finfish-algal aquaculture system. Aquaculture 252: 54–65.CrossRefGoogle Scholar
  15. Cole, K.M., Park, C.M., Reid, P.E. and Sheath, R.G. (1985). Comparative-studies on the cell-walls of sexual and asexual Bangia atropurpurea (Rhodophyta). 1. Histochemistry of polysaccharides. J. Phycol. 21: 585–592.CrossRefGoogle Scholar
  16. Cole, K.M. (1990) Chromosomes, In: K.M. Cole and R.G. Sheath (eds.) Biology of the Red Algae. Cambridge University Press, Cambridge, pp. 73–101.Google Scholar
  17. Collén, J., Del Río, M.J., García-Reina, G. and Pedersén, M. (1995) Photosynthetic H2O2 production by Ulva rigida. Planta 196: 225–230.CrossRefGoogle Scholar
  18. Croft, M.T., Lawrence, A.D., Raux, E., Warren, M.J. and Smith, A.G. (2005) Algae acquire vitamin B12 through a symbiotic relationship with bacteria. Nature 438: 90–93.PubMedCrossRefGoogle Scholar
  19. Cunningham, F.X. Jr., Lee, H. and Gantt, E. (2006) Carotenoid biosynthesis in the primitive red alga Cyanidioschyzon merolae. Eukaryot. Cell. 6: 533–545.PubMedCrossRefGoogle Scholar
  20. Dolganov, N.A., Bhaya, D. and Grossman A.R. (1995) Cyanobacterial protein with homology to the chlorophyll a/b binding proteins in higher plants: evolution and regulation. Proc. Natl. Acad. Sci. USA 92: 636–640.PubMedCrossRefGoogle Scholar
  21. Drew, K.M. (1949) Conchocelis-phase in the life history of Porphyra umbilicalis (L.) Kütz. Nature 164: 748–749.CrossRefGoogle Scholar
  22. Droop, M.R. (2007) Vitamins, phytoplankton and bacteria: symbiosis or scavenging? J. Plankton Res. 29: 107–113.CrossRefGoogle Scholar
  23. Fan, X., Fang, Y., Hu, S. and Wang, G. (2007) Generation and analysis of 5318 expressed sequence tags (ESTs) from the filamentous sporophyte of Porphyra haitanensis Ueda (Rhodophyta). J. Phycol. 43: 1287–1294. CrossRefGoogle Scholar
  24. Fukuda, S., Mikami, K., Uji, T., Park, E.-J., Ohba, T., Asada, K., Kitade, Y., Endo, H., Kato, I. and Saga, N. (2008) Factors influencing efficiency of transient gene expression in the red macrophyte Porphyra yezoensis. Plant Sci. 174: 329–339.CrossRefGoogle Scholar
  25. Gantt, E., Grabowski, B. and Cunningham, F.X. (2003) Antenna systems of red algae: phycobilisomes with photosystem II and chlorophyll complexes with photosystem I, In: B.R. Green and W.W. Parson (eds.) Light-Harvesting Antennas in Photosynthesis. Kluwer, Dordrecht, The Netherlands, pp. 307–322.Google Scholar
  26. Gretz, M.R., Aronson, J.M. and Sommerfeld, M.R. (1986) Cell-wall composition of the conchocelis phases of Bangia atropurpurea and Porphyra leucosticta (Rhodophyta). Botanica Marina. 29: 91–96.CrossRefGoogle Scholar
  27. Gross, J., Meurer, J. and Bhattacharya, D. (2008) Evidence of a chimeric genome in the cyanobacterial ancestor of plastids. BMC Evol. Biol. 8: 117–129.PubMedCrossRefGoogle Scholar
  28. Halliwell, B. and Gutteridge, J.M.C. (1999) Free Radicals in Biology and Medicine, 3rd edition. Oxford University Press, New York.Google Scholar
  29. Kafuku, T. and Ikenoue, H. (1983) Modern Methods of Aquaculture in Japan. Elsevier, Amsterdam.Google Scholar
  30. Kalanon, M. and McFadden, G.I. (2008) The chloroplast protein translocation complexes of Chlamydomonas reinhardtii: a bioinformatic comparison of Toc and Tic components in plants, green algae and red algae. Genetics 179: 95–112.PubMedCrossRefGoogle Scholar
  31. Kazazian, H.H. (2004) Mobile elements: drivers of genome evolution. Science 303: 1626–1632.PubMedCrossRefGoogle Scholar
  32. Keeling, P.J. and Palmer, J.D. (2008) Horizontal gene transfer in eukaryotic evolution. Nat. Rev. Genet. 9: 605–618.PubMedCrossRefGoogle Scholar
  33. Kidwell, M.G. (2002) Transposable elements and the evolution of genome size in eukaryotes. Genetica 115: 49–63.PubMedCrossRefGoogle Scholar
  34. Kim, J.K., Kraemer, G.P., Neefus, C.D., Chung, I.K. and Yarish, C. (2007) The effects of temperature and ammonium on growth, pigment production and nitrogen uptake in four species of Porphyra native to the coast of New England. J. Appl. Phycol. 19: 431–440.CrossRefGoogle Scholar
  35. Kitade, Y., Asamizu, E., Fukuda, S., Nakajima, M., Ootsuka, S., Endo, H., Tabata, S. and Saga, N. (2008) Identification of genes preferentially expressed during asexual sporulation in Porphyra yezoensis gametophytes (Bangiales, Rhodophyta). J. Phycol. 44: 113–123.CrossRefGoogle Scholar
  36. Knight, G.A. and Nelson, W.A. (1999) An evaluation of characters obtained from life history studies for distinguishing New Zealand Porphyra species. J. Appl. Phycol. 11: 411–419.CrossRefGoogle Scholar
  37. Kraemer, G.P., Carmona, R., Chopin, T., Neefus, C., Tang, X.R. and Yarish, C. (2004) Evaluation of the bioremediatory potential of several species of the red alga Porphyra using short-term measurements of nitrogen uptake as a rapid bioassay. J. Appl. Phycol. 16: 489–497.CrossRefGoogle Scholar
  38. Lee, E., Seo, S.B., Kim, T.H., Sung, S.K., An, G., Lee, C.H. and Kim, Y.J. (2000) Analysis of expressed sequence tags of Porphyra yezoensis. Mol. Cells 10: 338–342.PubMedGoogle Scholar
  39. Lee, R.E. and Fultz, S.A. (1970) Ultrastructure of the conchocelis stage of the marine red alga Porphyra leucosticta. J. Phycol. 6: 22–28.Google Scholar
  40. Le Gall, Y., Brown, S., Marie, D., Mejjad, M. and Kloareg, B. (1993) Quantification of nuclear DNA and G-C content in marine macroalgae by flow cytometry of isolated nuclei. Protoplasma 173: 123–132.CrossRefGoogle Scholar
  41. Lüning, K., Titlyanov, E.A. and Titlyanova, T.V. (1997) Diurnal and circadian periodicity of mitosis and growth in marine macroalgae. III. The red alga Porphyra umbilicalis. Eur. J. Phycol. 32: 167–173.Google Scholar
  42. Lüning, K. (2001) Circadian growth in Porphyra umbilicalis (Rhodophyta): spectral sensitivity of the circadian system. J. Phycol. 37: 52–58CrossRefGoogle Scholar
  43. MacArtain, P., Gill, C.I.R., Brooks, M., Campbell, R. and Rowland, I.R. (2007) Nutritional value of edible seaweeds. Nutr. Rev. 65: 535–543.PubMedCrossRefGoogle Scholar
  44. Marquardt, J. and Hanelt, D. (2004) Carotenoid composition of Delesseria lancifolia and other marine red algae from polar and temperate habitats. Eur. J. Phycol. 39: 285–292.CrossRefGoogle Scholar
  45. Masuda, T. (2008) Recent overview of the Mg branch of the tetrapyrrole biosynthesis leading to chlorophylls. Photosynth. Res. 96: 121–143.PubMedCrossRefGoogle Scholar
  46. Matsuzaki, M., Misumi, O., Shin-I, T., Maruyama, S., Takahara, M., Miyagishima, S.Y., Mori, T., Nishida, K., Yagisawa, F., Nishida, K., Yoshida, Y., Nishimura, Y., Nakao, S., Kobayashi, T., Momoyama, Y., Higashiyama, T., Minoda, A., Sano, M., Nomoto, H., Oishi, K., Hayashi, H., Ohta, F., Nishizaka, S., Haga, S., Miura, S., Morishita, T., Kabeya, Y., Terasawa, K., Suzuki, Y., Ishii, Y., Asakawa, S., Takano, H., Ohta, N., Kuroiwa, H., Tanaka, K., Shimizu, N., Sugano, S., Sato, N., Nozaki, H., Ogasawara, N., Kohara, Y. and Kuroiwa, T. (2004) Genome sequence of the ultrasmall unicellular red alga Cyanidioschyzon merolae 10D. Nature 428: 653–657.PubMedCrossRefGoogle Scholar
  47. Merchant, S.S., Prochnik, S.E., Vallon, O., Harris, E.H., Karpowicz, S.J., Witman, G.B., Terry, A., Salamov, A., Fritz-Laylin, L.K., Maréchal-Drouard, L., Marshall, W.F., Qu, L.H., Nelson, D.R., Sanderfoot, A.A., Spalding, M.H., Kapitonov, V.V., Ren, Q., Ferris, P., Lindquist, E., Shapiro, H., Lucas, S.M., Grimwood, J., Schmutz, J., Cardol, P., Cerutti, H., Chanfreau, G., Chen, C.L., Cognat, V., Croft, M.T., Dent, R., Dutcher, S., Fernández, E., Fukuzawa, H., González-Ballester, D., González-Halphen, D., Hallmann, A., Hanikenne, M., Hippler, M., Inwood, W., Jabbari, K., Kalanon, M., Kuras, R., Lefebvre, P.A., Lemaire, S.D., Lobanov, A.V., Lohr, M., Manuell, A., Meier, I., Mets, L., Mittag, M., Mittelmeier, T., Moroney, J.V., Moseley, J., Napoli, C., Nedelcu, A.M., Niyogi, K., Novoselov, S.V., Paulsen, I.T., Pazour, G., Purton, S., Ral, J.P., Riaño-Pachón, D.M., Riekhof, W., Rymarquis, L., Schroda, M., Stern, D., Umen, J., Willows, R., Wilson, N., Zimmer, S.L., Allmer, J., Balk, J., Bisova, K., Chen, C.J., Elias, M., Gendler, K., Hauser, C., Lamb, M.R., Ledford, H., Long, J.C., Minagawa, J., Page, M.D., Pan, J., Pootakham, W., Roje, S., Rose, A., Stahlberg, E., Terauchi, A.M., Yang, P., Ball, S., Bowler, C., Dieckmann, C.L., Gladyshev, V.N., Green, P., Jorgensen, R., Mayfield, S., Mueller-Roeber, B., Rajamani, S,, Sayre, R.T., Brokstein, P., Dubchak, I., Goodstein, D., Hornick, L., Huang, Y.W., Jhaveri, J., Luo, Y., Martínez, D., Ngau, W.C., Otillar, B., Poliakov, A., Porter, A., Szajkowski, L., Werner, G., Zhou, K., Grigoriev, I.V., Rokhsar, D.S. and Grossman, A.R. (2007) The Chlamydomonas genome reveals the evolution of key animal and plant functions. Science 318: 245–251.PubMedCrossRefGoogle Scholar
  48. Minocha, S.C., Hunt, M. and Mathews, D.E. (2008) Molecular and biochemical characterization of four genes involved in sulfur metabolism in Porphyra purpurea. J. Appl. Phycol. 333–345.Google Scholar
  49. Mitman, G. and van der Merr, J.P. (1994) Meiosis, blade development, and sex determination in Porphyra purpurea (Rhodophyta). J. Phycol. 30: 1–17.CrossRefGoogle Scholar
  50. Miura, A. (1990) Present trends and perspective in Porphyra (nori) breeding. Genetics of pigmentation mutants in Porphyra yezoensis: developmental origin of variegated gametophytic thalli. Suisan Ikushu 15: 19–30 (in Japanese, a review).Google Scholar
  51. Müller, K.M., Ellenor, D.W., Sherwood, A.R., Sheath, R.G., Cannone, J.J. and Gutell, R.R. (2005) Evidence for lateral transfer of an IE intron between fungal and red algal small subunit rRNA genes. J. Phycol. 41: 380–390.CrossRefGoogle Scholar
  52. Mukai, L.S., Craigie, J.S. and Brown, R.G. (1981) Chemical-composition and structure of the cell-walls of the conchocelis and thallus phases of Porphyra tenera (Rhodophyceae). J. Phycol. 17: 192–198.CrossRefGoogle Scholar
  53. Nelson, W.A., Brodie, J. and Guiry, M.D. (1999) Terminology used to describe reproduction and life history stages in the genus Porphyra (Bangiales, Rhodophyta). J. Appl. Phycol. 11: 407–410.CrossRefGoogle Scholar
  54. Nelson, W.A., Farr, T.J. and Broom, J.E.S. (2006) Phylogenetic relationships and generic concepts in the red order Bangiales: challenges ahead. Phycologia 45: 249–259.CrossRefGoogle Scholar
  55. Nikaido, I., Asamizu, E., Nakajima, M., Nakamura, Y., Saga, N. and Tabata, S. (2000) Generation of 10,154 expressed sequence tags from a leafy gametophyte of a marine red alga, Porphyra yezoensis. DNA Res. 7: 223–227.PubMedCrossRefGoogle Scholar
  56. Niwa, K., Miura, A., Shin, J.-A. and Aruga, Y. (1993) Characterization and genetic analysis of the violet type pigmentation mutant of Porphyra yezoensis Ueda (Bangiales, Rhodophyta). Kor. J. Phycol. 8: 217–230.Google Scholar
  57. Noda, H. (1993) Health benefits and nutritional properties of nori. J. Appl. Phycol. 5: 255–258.CrossRefGoogle Scholar
  58. Nozaki, H., Takano, H., Misumi, O., Terasawa, K., Matsuzaki, M., Maruyama, S., Nishida, K., Yagisawa, F., Yoshida, Y., Fujiwara, T., Takio, S., Tamura, K., Chung, S.J., Nakamura, S., Kuroiwa, H., Tanaka, K., Sato, N. and Kuroiwa, T. (2007) A 100%-complete sequence reveals unusually simple genomic features in the hot-spring red alga Cyanidioschyzon merolae. BMC Biol. 5: 28.PubMedCrossRefGoogle Scholar
  59. Ohta, N., Matsuzaki, M., Misumi, O., Miyagsishima, S.-A., Nozaki, H., Tanaka, K., Shin-I, T., Kohara, Y. and Kuroiwa, T. (2003) Complete sequence and analysis of the plastid genome of the unicellular red alga Cyanidioschyzon merolae. DNA Res. 10: 67–77.PubMedCrossRefGoogle Scholar
  60. Oliveira, M.C., Kurniawan, J., Bird, C.L., Rice, E.L., Murphy, C.A., Singh, R.K., Gutell, R.R. and Ragan, M.A. (1995) A preliminary investigation of the order Bangiales (Bangiophycidae, Rhodophyta) based on sequences of nuclear small-subunit ribosomal RNA genes. Phycol. Res. 43: 71–79.CrossRefGoogle Scholar
  61. Pearson, G., Serrão, E.A. and Cancela, M.L. (2001) Suppression subtractive hybridization for studying gene expression during aerial exposure and desiccation in fucoid algae. Eur. J. Phycol. 36: 359–366.CrossRefGoogle Scholar
  62. Pickett-Heaps, J., West, J.A., Wilson, S.M. and McBride, D. (2001) Time-lapse videomicroscopy of cell (spore) movement in red algae. Eur. J. Phycol. 36: 9–22.CrossRefGoogle Scholar
  63. Pueschel, C.M. (1994) Systematic significance of the absence of pit-plug cap membranes in the Batrachospermales (Rhodophyta). J. Phycol. 30: 310–315.CrossRefGoogle Scholar
  64. Reith, M. and Munholland, J. (1995) Complete nucleotide sequence of the Porphyra purpurea chloroplast genome. Plant Mol. Biol. Rep. 13: 33–335CrossRefGoogle Scholar
  65. Reyes-Prieto, A. and Bhattacharya, D. (2007) Phylogeny of Calvin cycle enzymes supports Plantae monophyly. Mol. Phylogenet. Evol. 45: 384–391.PubMedCrossRefGoogle Scholar
  66. Reyes-Prieto, A., Weber, A.P.N. and Bhattacharya, D. (2007) The origin and establishment of the plastid in algae and plants. Annu. Rev. Genet. 41: 147–168.PubMedCrossRefGoogle Scholar
  67. Sampath-Wiley, P., Neefus, C.D. and Jahnke, L.S. (2008) Seasonal effects of sun exposure and emersion on intertidal seaweed physiology: fluctuations in antioxidant contents, photosynthetic pigments and photosynthetic efficiency in the red alga Porphyra umbilicalis Kützing (Rhodophyta, Bangiales). J. Exp. Mar. Biol. Ecol. 361: 83–91.CrossRefGoogle Scholar
  68. Shick, J.M. and Dunlap, W.C. (2002) Mycosporine-like amino acids and related gadusols: biosynthesis, accumulation, and UV-protective functions in aquatic organisms. Annu. Rev. Physiol. 64: 223–262.PubMedCrossRefGoogle Scholar
  69. Schubert, N., Garcia-Mendoza, E. and Pacheco-Ruiz, I. (2006) Carotenoid composition of marine red algae. J. Phycol. 42: 1208–1216.CrossRefGoogle Scholar
  70. Shimma, Y. and Taguchi, H. (1966) Studies on lipids of “nori”, dry seaweed – III. Carotenoid components. Nippon Suisan Gakkai. 32: 1031–1036.CrossRefGoogle Scholar
  71. Sinha, R.P., Singh, S.P. and Häder, D.P. (2007) Database on mycosporines and mycosporine-like amino acids (MAAs) in fungi, cyanobacteria, macroalgae, phytoplankton and animals. J. Photochem. Photobiol. B Biol. 80: 29–35.CrossRefGoogle Scholar
  72. Takano, S., Nakanishi, A., Uernura, D. and Hirata, Y. (1979) Isolation and structure of a 334 nm UV-absorbing substance, porphyra-334 from the red alga Porphyra tenera Kjellman. Chem. Lett. 26: 419–420CrossRefGoogle Scholar
  73. Takeda, A., Iwasaki, S., Watanabe, T., Utsumi, M. and Watanabe, Y. (2008) The mechanism selecting the guide strand from small RNA duplexes is different among argonaute proteins. Plant Cell Physiol. 49: 493–500.PubMedCrossRefGoogle Scholar
  74. Takenaka, S., Takubo, K., Watanabe, F., Tanno, T., Tsuyama, S., Nanano, Y. and Tamura, Y. (2003) Occurrence of coenzyme forms of Vitamin B12 in a cultured purple laver (Porphyra yezoensis). Biosci. Biotechnol. Biochem. 67: 2480–2482.PubMedCrossRefGoogle Scholar
  75. Tseng, C.K. (1981) Commercial Cultivation, In: C.S. Lobban and M.J. Wynne (eds.) The Biology of Seaweeds. Blackwell, Oxford, pp. 680–725.Google Scholar
  76. Ueki, C., Nagasato C., Motomura, T. and Saga, N. (2008) Reexamination of the pit plugs and the characteristic membranous structures in Porphyra yezoensis (Bangiales, Rhodophyta). Phycologia 47: 5–11.CrossRefGoogle Scholar
  77. Uppalapati, S.R. and Fujita, Y. (2000) Carbohydrate regulation of attachment, encystment, and appressorium formation by Pythium porphyrae (Oomycota) zoospores on Porphyra yezoensis (Rhodophyta). J Phycol. 36: 359–366.CrossRefGoogle Scholar
  78. Vazquez, F. (2006) Arabidopsis endogenous small RNAs: highways and byways. Trends Plant Sci. 11: 460–468.PubMedCrossRefGoogle Scholar
  79. Viola, R., Nyvall, P. and Pedersen, M. (2001) The unique features of starch metabolism in red algae. Proc. R. Soc. Lond. Biol. Sci. 268: 1417–1422.CrossRefGoogle Scholar
  80. Wilkes, R.J., Yarish, C. and Mitman, G.G. (1999) Observations on the chromosome numbers of Porphyra (Bangiales, Rhodophyta) populations from Long Island Sound to the Canadian Maritimes. Algae 14: 219–222.Google Scholar
  81. Wolfe, G.R., Cunningham, F.X., Durnford, D., Green, B.R. and Gantt, E. (1994) Evidence for a common origin of chloroplasts with light-harvesting complexes of different pigmentation. Nature 367: 566–568.CrossRefGoogle Scholar
  82. Wu, L. and Belasco, J.G. (2008) Let me count the ways: mechanisms of gene regulation by miRNAs and siRNAs. Mol. Cell. 29: 1–7.PubMedCrossRefGoogle Scholar
  83. Yarish, C. and Pereira, R. (2008) Mass production of marine macroalgae, In S.E. Jørgensen and B.D. Fath (eds.) Ecological Engineering. Vol. 3. Encyclopedia of Ecology. Elsevier, Oxford, pp. 2236–2247.Google Scholar
  84. Yoon, H.S., Müller, K.M., Sheath, R.G., Ott, F.D. and Bhattacharya, D. (2006) Defining the major lineages of red algae (Rhodophyta). J. Phycol. 42: 482–492.CrossRefGoogle Scholar
  85. Zhang, X.-C., Qin, S., Ma, J.-H. and Xu, P. (2005) The Genetics of Marine Algae. Chinese Agricultural Press, Beijing (in Chinese).Google Scholar

Copyright information

© Springer Science+Business Media B.V. 2010

Authors and Affiliations

  • Elisabeth Gantt
    • 1
  • G. Mine Berg
    • 2
  • Debashish Bhattacharya
    • 3
  • Nicolas A. Blouin
    • 4
  • Juliet A. Brodie
    • 5
  • Cheong Xin Chan
    • 3
  • Jonas Collén
    • 6
  • Francis X. CunninghamJr
    • 1
  • Jeferson Gross
    • 3
  • Arthur R. Grossman
    • 7
  • Steven Karpowicz
    • 8
  • Yukihiro Kitade
    • 9
  • Anita S. Klein
    • 10
  • Ira A. Levine
    • 11
  • Senjie Lin
    • 12
  • Shan Lu
    • 13
  • Michael Lynch
    • 14
  • Subhash C. Minocha
    • 10
  • Kirsten Müller
    • 14
  • Christopher D. Neefus
    • 10
  • Mariana Cabral de Oliveira
    • 15
  • Linda Rymarquis
    • 16
  • Alison Smith
    • 17
  • John W. Stiller
    • 18
  • Wen-Kai Wu
    • 19
  • Charles Yarish
    • 20
  • Yun Zhuang
    • 12
  • Susan H. Brawley
    • 4
  1. 1.Department of Cell Biology and Molecular GeneticsUniversity of MarylandCollege ParkUSA
  2. 2.Department of GeophysicsStanford UniversityStanfordUSA
  3. 3.Department of Ecology, Evolution and Natural ResourcesRutgers UniversityNew BrunswickUSA
  4. 4.Department of Marine SciencesUniversity of MaineOronoUSA
  5. 5.Department of BotanyThe Natural History MuseumLondonUK
  6. 6.CNRSUniversité Pierre et Marie Curie, Station BiologiqueRoscoff, cedexFrance
  7. 7.Department of Plant BiologyThe Carnegie InstitutionStanfordUSA
  8. 8.Department of ChemistryUniversity of CaliforniaLos AngelesUSA
  9. 9.Algal Genetics and Chemistry, Fisheries SciencesHokkaido UniversityHakodateJapan
  10. 10.Department of Biological SciencesUniversity of New HampshireDurhamUSA
  11. 11.Natural and Applied SciencesUniversity of Southern MaineLewistonUSA
  12. 12.Department of Marine SciencesUniversity of ConnecticutGrotonUSA
  13. 13.School of Life SciencesNanjing UniversityNanjingChina
  14. 14.Department of BiologyUniversity of WaterlooWaterlooCA
  15. 15.Department of Botany, Biosciences InstituteUniversity of São PauloSão PauloBrazil
  16. 16.Biotechnology InstituteUniversity of DelawareNewarkUSA
  17. 17.Department of Plant SciencesUniversity CambridgeCambridgeUK
  18. 18.Department of BiologyEast Carolina UniversityGreenvilleUK
  19. 19.College of Fisheries and Life ScienceShanghai Ocean UniversityShanghaiCN
  20. 20.Department of Ecology & Evolutionary BiologyUniversity of ConnecticutStamfordUSA

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