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).
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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.
Bendall D S, Manasse R S. 1995. Cyclic photophosphorylation and electron transport. Biochim. Biophys. Acta, 1229: 23–38.
Chapple C. 1998. Molecular genetics analysis of plant cytochrome P450-dependent monooxygenases. Annu. Rev. Plant Physiol. Plant Mol. Biol., 49: 311–343.
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.
Croft M T, Warren M J, Smith A G. 2006. Algae need their vitamins. Eukaryotic Cell, 5: 1 175–1 183.
Delledonne M. 2005. NO news is good news for plants. Curr. Opin. Plant Biol., 8: 390–396.
Duarte C M. 1995. Submerged aquatic vegetation in relation to different nutrient regimes. Ophelia, 41: 87–112.
Ewing B, Green P. 1998a. Base-calling of automated sequencer traces using phred II Error probabilities. Genome Res., 8: 186–194.
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.
Felsenstein J. 1993. PHYLIP (Phylogeny Inference Package) version 35c. Distributed by the author Seattle, Department of Genetics, University of Washington, Washington.
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.
Fletcher R T. 1996. Marine Benthic Vegetation-Recent Changes and the Effects of Eutrophication: The occurrence of ‘green-tide’. Springer Verlag, Berlin.
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.
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.
Gordon D, Abajian C, Green P. 1998. Consed: a graphical tool for sequence finishing. Genome Res., 8: 195–202.
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.
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.
Im C S, Grossman A R. 2002. Identification and regulation of high lightinduced genes in Chlamydomonas reinhardtii. Plant J., 30: 301–313.
Hiraoka M, Ohno M, Kawaguchi S, Yoshida G. 2004. Crossing test among floating Ulva thalli forming ‘green-tide’ in Japan. Hydrobiologia, 512: 239–245.
Kanehisa M, Goto S. 2000. KEGG: Kyoto encyclopedia of genes and genomes. Nucleic Acids Res., 28: 27–30.
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.
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.
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.
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.
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.
Mittler R, Vanderauwera S, Gollery M, Van Breusegem F. 2004. The reactive oxygen gene network in plants. Trends Plant Sci., 9: 490–498.
Miyake C, Asada K. 1994. Ferredoxin-dependent photoreduction of the monodehydroascorbate radical in spinach thylakoids. Plant Cell Physiol., 35: 539–549.
Morand P, Briand X. 1996. Excessive growth of macroalgae: a symptom of environmental disturbance. Bot. Mar., 39: 491–516.
Morand P, Merceron M. 2005. Macroalgal population and sustainability. J. Coastal. Res., 21: 1 009–1 020.
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.
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.
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.
Page R D M. 1996. TREEVIEW: an application to display phylogenetic trees on personal computers. Computer Applied Bioscience, 12: 357–358.
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.
Pickart C M. 2001. Mechanisms underlying ubiquitination. Annu. Rev. Biochem., 70: 503–533.
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.
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.
Schuler M A. 1996. Plant cytochrome P450 monooxygenases. Crit. Rev. Plant Sci., 15: 235–284.
Schuler M A, Werck-Reichhart D. 2003. Functional genomics of P450s. Annu. Rev. Plant Biol., 54: 629–667.
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.
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.
The Gene Ontology Consortium. 2000. Gene Ontology: tool for the unification of biology. Nat. Genet., 25: 25–29.
The Gene Ontology Consortium. 2004. The Gene Ontology (GO) database and informatics resource. Nucleic Acids Res., 32: 258–261.
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.
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.
Tortell P D, Reinfelder J R, Morel F M M. 1997. Active uptake of bicarbonate by diatoms. Nature, 390: 243–244.
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.
Vranová E, Inzé D, Van Breusegem F. 2002. Signal transduction during oxidative stress. J. Exp. Bot., 53: 1 227–1 236.
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)
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.
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Supported by the Scientific and Technical Supporting Programs of China (2008BAC49B01), the National Natural Science Foundation of China (No. 30830015)
NIU Jianfeng and HU Haiyan contributed equally to this publication.
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Niu, J., Hu, H., Hu, S. et al. Analysis of expressed sequence tags from the Ulva prolifera (Chlorophyta). Chin. J. Ocean. Limnol. 28, 26–36 (2010). https://doi.org/10.1007/s00343-010-9120-4
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DOI: https://doi.org/10.1007/s00343-010-9120-4