Chinese Journal of Oceanology and Limnology

, Volume 28, Issue 1, pp 26–36 | Cite as

Analysis of expressed sequence tags from the Ulva prolifera (Chlorophyta)

  • Jianfeng Niu (牛建峰)
  • Haiyan Hu (胡海岩)
  • Songnian Hu (胡松年)
  • Guangce Wang (王广策)
  • Guang Peng (彭光)
  • Song Sun (孙 松)
Biology

Abstract

In 2008, a green tide broke out before the sailing competition of the 29th Olympic Games in Qingdao. The causative species was determined to be Enteromorpha prolifera (Ulva prolifera O. F. Müller), a familiar green macroalga along the coastline of China. Rapid accumulation of a large biomass of floating U. prolifera prompted research on different aspects of this species. In this study, we constructed a nonnormalized cDNA library from the thalli of U. prolifera and acquired 10 072 high-quality expressed sequence tags (ESTs). These ESTs were assembled into 3 519 nonredundant gene groups, including 1 446 clusters and 2 073 singletons. After annotation with the nr database, a large number of genes were found to be related with chloroplast and ribosomal protein, GO functional classification showed 1 418 ESTs participated in photosynthesis and 1 359 ESTs were responsible for the generation of precursor metabolites and energy. In addition, rather comprehensive carbon fixation pathways were found in U. prolifera using KEGG. Some stress-related and signal transduction-related genes were also found in this study. All the evidences displayed that U. prolifera had substance and energy foundation for the intense photosynthesis and the rapid proliferation. Phylogenetic analysis of cytochrome c oxidase subunit I revealed that this green-tide causative species is most closely affiliated to Pseudendoclonium akinetum (Ulvophyceae).

Keyword

green tide Ulva Prolifera expressed sequence tag (EST) filamentous green alga rapid growth proliferation 

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References

  1. Altschul S F, Madden T L, Schaffer A A, Zhang J, Zhang Z, Miller W, Lipman D J. 1997. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res., 25: 3 389–3 402.CrossRefGoogle Scholar
  2. Bendall D S, Manasse R S. 1995. Cyclic photophosphorylation and electron transport. Biochim. Biophys. Acta, 1229: 23–38.CrossRefGoogle Scholar
  3. Chapple C. 1998. Molecular genetics analysis of plant cytochrome P450-dependent monooxygenases. Annu. Rev. Plant Physiol. Plant Mol. Biol., 49: 311–343.CrossRefGoogle Scholar
  4. Clark D, Durner J, Navarre D A, Klessig D F. 2000. Nitric oxide inhibition of tobacco catalase and ascorbate peroxidase. Mol. Plant-Microbe Interact., 13: 1 380–1 384.CrossRefGoogle Scholar
  5. Croft M T, Warren M J, Smith A G. 2006. Algae need their vitamins. Eukaryotic Cell, 5: 1 175–1 183.CrossRefGoogle Scholar
  6. Delledonne M. 2005. NO news is good news for plants. Curr. Opin. Plant Biol., 8: 390–396.CrossRefGoogle Scholar
  7. Duarte C M. 1995. Submerged aquatic vegetation in relation to different nutrient regimes. Ophelia, 41: 87–112.Google Scholar
  8. Ewing B, Green P. 1998a. Base-calling of automated sequencer traces using phred II Error probabilities. Genome Res., 8: 186–194.Google Scholar
  9. Ewing B, Hillier L, Wendl M C, Green P. 1998b. Base-calling of automated sequencer traces using phred I Accuracy assessment. Genome Res., 8: 175–185.Google Scholar
  10. Felsenstein J. 1993. PHYLIP (Phylogeny Inference Package) version 35c. Distributed by the author Seattle, Department of Genetics, University of Washington, Washington.Google Scholar
  11. Finazzi G. 2005. The central role of the green alga Chlamydomonas reinhardtii in revealing the mechanism of state transitions. J. Exp. Bot., 56: 383–388.CrossRefGoogle Scholar
  12. Fletcher R T. 1996. Marine Benthic Vegetation-Recent Changes and the Effects of Eutrophication: The occurrence of ‘green-tide’. Springer Verlag, Berlin.Google Scholar
  13. Fong P, Donohoe R M, Zedler J B. 1994. Nutrient concentration in tissue of the macroalga Enteromorpha as a function of nutrient history: An experimental evaluation using field microcosms. Mar. Ecol. Prog. Ser., 106: 273–281.CrossRefGoogle Scholar
  14. Fujita R M. 1985. The role of nitrogen status in regulating transient ammonium uptake and nitrogen storage by macroalgae. J. Exp. Mar. Bio. Ecol., 92: 283–301.CrossRefGoogle Scholar
  15. Gordon D, Abajian C, Green P. 1998. Consed: a graphical tool for sequence finishing. Genome Res., 8: 195–202.Google Scholar
  16. Hayden H S, Blomster J, Maggs C A, Silva P C, Stanhope M J, Waalland J R. 2003. Linnaeus was right all along: Ulva and Enteromorpha are not distinct genera. Eur. J. Phycol., 38: 277–294.CrossRefGoogle Scholar
  17. Henry I M, Wilkinson M D, Hernandez J M, Schwarz-Sommer Z, Grotewold E, Mandoli D F. 2004. Comparison of ESTs from juvenile and adult phases of the giant unicellular green alga Acetabularia acetabulum. BMC Plant Biology, 4: 3.CrossRefGoogle Scholar
  18. Im C S, Grossman A R. 2002. Identification and regulation of high lightinduced genes in Chlamydomonas reinhardtii. Plant J., 30: 301–313.CrossRefGoogle Scholar
  19. Hiraoka M, Ohno M, Kawaguchi S, Yoshida G. 2004. Crossing test among floating Ulva thalli forming ‘green-tide’ in Japan. Hydrobiologia, 512: 239–245.CrossRefGoogle Scholar
  20. Kanehisa M, Goto S. 2000. KEGG: Kyoto encyclopedia of genes and genomes. Nucleic Acids Res., 28: 27–30.CrossRefGoogle Scholar
  21. Liang Z Y, Lin X Z, Ma M, Zhang J, Yan X B, Liu T. 2008. A preliminary study of the Enteromorpha prolifera drift gathering causing the Green Tide phenomenon. Period Ocean Univ. China, 38: 601–604.Google Scholar
  22. Lin A P, Shen S D, Wang J W, Yan B L. 2008. Reproduction diversity of Enteromorpha prolifera. J. Integr. Plant Biol., 50: 622–629.CrossRefGoogle Scholar
  23. Martins I, Pardal M A, Lillebo A I, Flindt M R, Marques J C. 2001. Hydrodynamics as a major factor controlling the occurrence of green macroalgal blooms in a eutrophic estuary: A case study on the influence of precipitation and river management. Estuar. Coast. Shelf Sci., 52: 165–177.CrossRefGoogle Scholar
  24. Merceron M, Antoine V, Auby I, Morand P. 2007. In situ growth potential of the subtidal part of green-tide forming Ulva spp.. Stocks. Sci. Total Environ., 384: 293–305.CrossRefGoogle Scholar
  25. Miklós S, Németh K, Koncz-Kálmán Z, Mathur J, Kauschmann A, Altmann T, Rédei G P, Nagy F, Schell J, Koncz C. 1996. Brassinosteroids rescue the deficiency of CYP90, a cytochrome P450, controlling cell elongation and de-etiolation in Arabidopsis. Cell, 85: 171–182.CrossRefGoogle Scholar
  26. Mittler R, Vanderauwera S, Gollery M, Van Breusegem F. 2004. The reactive oxygen gene network in plants. Trends Plant Sci., 9: 490–498.CrossRefGoogle Scholar
  27. Miyake C, Asada K. 1994. Ferredoxin-dependent photoreduction of the monodehydroascorbate radical in spinach thylakoids. Plant Cell Physiol., 35: 539–549.Google Scholar
  28. Morand P, Briand X. 1996. Excessive growth of macroalgae: a symptom of environmental disturbance. Bot. Mar., 39: 491–516.CrossRefGoogle Scholar
  29. Morand P, Merceron M. 2005. Macroalgal population and sustainability. J. Coastal. Res., 21: 1 009–1 020.CrossRefGoogle Scholar
  30. Mulder N J, Apweiler R, Attwood T K, Bairoch A, Barrell D, Bateman A, Binns D, Biswas M, Bradley P, Bucher P, Copley R R, Courcelle E, Das U, Durbin R, Falquet L, Fleischmann W, Griffiths-Jones S, Haft D, Harte N, Hulo N, Kahn D, Kanapin A, Krestyaninova M, Lopez R, Letunic I, Lonsdale D, Silventoinen V, Orchard S E, Pagni M, Peyruc D, Ponting C P, Selengut J D, Servant F, Sigrist C J A, Vaughan R, Zdobnov E M. 2003. The interpro database, 2003 brings increased coverage and new features. Nucleic Acids Res., 31: 315–318.CrossRefGoogle Scholar
  31. Nedelcu A M, Lee R W, Lemieux C, Gray M W, Burger G. 2000. The complete mitochondrial DNA sequence of Scenedesmus obliquus reflects an intermediate stage in the evolution of the green algal mitochondrial genome. Genome Res., 10: 819–831.CrossRefGoogle Scholar
  32. Ogawa T. 1991. A gene homologous to the subunit-2 gene of NADH dehydrogenase is essential to inorganic carbon transport of Synechocystis PCC6803. Proc. Natl. Acad. Sci., 88: 4 275–4 279.Google Scholar
  33. Page R D M. 1996. TREEVIEW: an application to display phylogenetic trees on personal computers. Computer Applied Bioscience, 12: 357–358.Google Scholar
  34. Paquette S M, Bak S, Feyereisen R. 2000. Intron-exon organization and phylogeny in a large superfamily, the paralogous cytochrome P450 genes of Arabidopsis thaliana DNA. Cell Biol., 19: 307–317.Google Scholar
  35. Pickart C M. 2001. Mechanisms underlying ubiquitination. Annu. Rev. Biochem., 70: 503–533.CrossRefGoogle Scholar
  36. Raffaelli D, Balls P, Way S, Patterson I J, Honmann S, Corp N. 1999. Major long-term changes in the ecology of the Ythan estuary, Aberdeenshire, Scotland; How important are physical factors? Aquat. Conserv., 9: 219–236.CrossRefGoogle Scholar
  37. Reiskind J B, Bowes G. 1991. The role of phosphoenolpyruvate carboxykinase in a marine macroalga with C4-like photosynthetic characteristics. Proc. Natl. Acad. Sci. USA, 88: 2 883–2 887.CrossRefGoogle Scholar
  38. Schuler M A. 1996. Plant cytochrome P450 monooxygenases. Crit. Rev. Plant Sci., 15: 235–284.CrossRefGoogle Scholar
  39. Schuler M A, Werck-Reichhart D. 2003. Functional genomics of P450s. Annu. Rev. Plant Biol., 54: 629–667.CrossRefGoogle Scholar
  40. Sfriso A, Marcomini A, Pavoni B. 1987. Relationships between macroalgal biomass and nutrient concentrations in a hypertroptfic area of the Venice Lagoon Italy. Marine Enviroumental Research, 22: 297–312.CrossRefGoogle Scholar
  41. Sun S, Wang F, Li C L, Qin S, Zhou M J, Ding L P, Pang S J, Duan D L, Wang G C, Yin B S, Yu R C, Jiang P, Liu Z L, Zhang G T, Fei X G, Zhou M. 2008. Emerging challenges: Massive green algae blooms in the Yellow Sea. Nature Proceedings: hdl:10101/npre200822661.Google Scholar
  42. The Gene Ontology Consortium. 2000. Gene Ontology: tool for the unification of biology. Nat. Genet., 25: 25–29.CrossRefGoogle Scholar
  43. The Gene Ontology Consortium. 2004. The Gene Ontology (GO) database and informatics resource. Nucleic Acids Res., 32: 258–261.CrossRefGoogle Scholar
  44. Thompson J D, Gibson T J, Plewniak F, Jeanmougin F, Higgins D G. 1997. The ClustalX windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res., 25: 4 876–874 882.CrossRefGoogle Scholar
  45. Tian L, Musetti V, Kim J, Magallanes-Lundback M, DellaPenna D. 2004. The Arabidopsis LUT1 locus encodes a member of the cytochrome P450 family that is required for carotenoid epsilon-ring hydroxylation activity. Proc. Natl. Acad. Sci. USA, 101: 402–407.CrossRefGoogle Scholar
  46. Tortell P D, Reinfelder J R, Morel F M M. 1997. Active uptake of bicarbonate by diatoms. Nature, 390: 243–244.CrossRefGoogle Scholar
  47. Valiela I, McClelland J, Hauxwell J, Behr P J, Hersh D, Foreman K. 1997. Macroalgal blooms in shallow estuaries: controls and ecophysiological and ecosystem consequences. Limnol. Oceanogr., 42: 1 105–1 118.CrossRefGoogle Scholar
  48. Vranová E, Inzé D, Van Breusegem F. 2002. Signal transduction during oxidative stress. J. Exp. Bot., 53: 1 227–1 236.CrossRefGoogle Scholar
  49. Wang X K, Ma J H, Ye D C. 2007. Preliminary study on the life History of Enteromorpha prolifera. Mar. Sci. Bull., 26: 112–116. (In Chinese with English abstract)Google Scholar
  50. Wang Y, Ladunga I, Miller A R, M Horken K, Plucinak T, Weeks D P, Bailey C P. 2008. The Small Ubiquitin-Like Modifier (SUMO) and SUMO-Conjugating System of Chlamydomonas reinhardtii. Genetics, 179: 177–192.CrossRefGoogle Scholar

Copyright information

© Chinese Society for Oceanology and Limnology, Science Press and Springer Berlin Heidelberg 2010

Authors and Affiliations

  • Jianfeng Niu (牛建峰)
    • 1
  • Haiyan Hu (胡海岩)
    • 2
    • 4
  • Songnian Hu (胡松年)
    • 2
  • Guangce Wang (王广策)
    • 1
    • 3
  • Guang Peng (彭光)
    • 1
  • Song Sun (孙 松)
    • 1
  1. 1.Key Laboratory of Experimental Marine Biology, Institute of OceanologyChinese Academy of SciencesQingdaoChina
  2. 2.Key Laboratory of Genome Sciences and Information, Beijing Institute of GenomicsChinese Academy of SciencesBeijingChina
  3. 3.College of Marine Science and EngineeringTianjin University of Science and TechnologyTianjinChina
  4. 4.Graduate University of Chinese Academy of SciencesBeijingChina

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