Abstract
Ulvacean green seaweeds are common worldwide; they formed massive green tides in the Yellow Sea in recent years, which caused marine ecological problems as well as a social issue. We investigated two major genera of the Ulvaceae, Ulva and Enteromorpha, and collected the plastid rbcL and nuclear ITS sequences of specimens of the genera in two sides of the Yellow Sea and analyzed them. Phylogenetic trees of rbcL data show the occurrence of five species of Enteromorpha (E. compressa, E. flexuosa, E. intestinalis, E. linza and E. prolifera) and three species of Ulva (U. pertusa, U. rigida and U. ohnoi). However, we found U. ohnoi, which is known as a subtropical to tropical species, at two sites on Jeju Island, Korea. Four ribotypes in partial sequences of 5.8S rDNA and ITS2 from E. compressa were also found. Ribotype network analysis revealed that the common ribotype, occurring in China, Korea and Europe, is connected with ribotypes from Europe and China/Japan. Although samples of the same species were collected from both sides of the Yellow Sea, intraspecific genetic polymorphism of each species was low among samples collected worldwide.
Similar content being viewed by others
References
Bäck S, Lehvo A, Blomster J. 2000. Mass occurrence of unattached Enteromorpha intestinalis on the Finnish Baltic Sea coast. Ann. Bot. Fennici., 37: 155–161.
Bliding C. 1968. A critical survey of European taxa in Ulvales. II. Ulva, Ulvaria, Monostroma, Kornmannia. Bot. Not., 121: 534–629.
Blomster J, Bäck S, Fewer D P, Kiirikki M, Lehvo A, Maggs C A, Stanhope M J. 2002. Novel morphology in Enteromorpha (Ulvophyceae) forming green tides. Am. J. Bot., 89: 1 756–1 763.
Blomster J, Hoey E M, Maggs C A, Stanhope M J. 2000. Species-specific oligonucleotide probes for macroalgae: molecular discrimination of two marine fouling species of Enteromorpha (Chlorophyceae). Mol. Ecol., 9: 177–186.
Blomster J, Maggs C A, Stanhope M J. 1998. Molecular and morphological analysis of Enteromorpha intestinalis and E. compressa (Chlorophyta) in the British Isles. J. Phycol., 34: 319–340.
Cho T O, Boo S M. 1996. Seasonal changes of marine plants in Oeyondo Islands on the Yellow Sea. Algae, 11: 285–293.
Cho T O, Boo S M. 1998. Marine flora of Oeyondo Islands on the Yellow Sea, Korea: I. Green algae and seagrasses. Algae, 13: 1–11.
Clement M, Posada D, Crandall K A. 2000. TCS: a computer program to estimate gene genealogies. Mol. Ecol., 9: 1657–1660.
Dong M. 1963. A preliminary phytogeographical studies on Chinese species of Enteromorpha. Oceanol. et Limnol. Sin., 5: 46–51. (in Chinese)
Doyle J J, Doyle J L. 1990. Isolation of plant DNA from fresh tissue. Focus, 12: 13–15.
Fletcher R L, Cuomo V, Palomba I. 1990. The “green tide” problem, with particular reference to the Venice Lagoon. Br. Phycol. J., 25: 87.
Guiry M D, Dhonncha E N. 2002. AlgaeBase: http://www.algaebase.com.
Hall T A. 1999. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp. Ser., 41: 95–98.
Hayden H S, Waaland J R. 2002. Phylogenetic systematics of the Ulvaceae (Ulvales, Ulvophyceae) using chloroplast and nuclear DNA sequences. J. Phycol., 38: 1 200–1 212.
Hayden H S, Waaland J R. 2004. A molecular systematic study of Ulva (Ulvaceae, Ulvales) from the northeast Pacific. Phycologia, 43: 364–382.
Hayden H S, Blomster J, Maggs C A, Silva P C, Stanhope M J, Waaland J R. 2003. Linnaeus was right all along: Ulva and Enteromorpha are not distinct genera. Eur. J. Phycol., 38: 277–294.
Hiraoka M, Shimada S, Uenosono M, Masuda M. 2003. A new green-tide-forming alga, Ulva ohnoi Hiraoka et Shimada sp. Nov. (Ulvales, Ulvophyceae) from Japan. Phycol. Res., 51: 17–29.
Ichikawa H, Beardsley R. 2002. The current system in the Yellow and East China Seas. J. Oceanogr., 58: 77–92.
Jiang P, Wang J F, Cui Y L, Li Y X, Lin H Z, Qin S. 2008. Molecular phylogenetic analysis of attached Ulvaceae species and free-floating Enteromorpha from Qingdao coasts in 2007. Chin. J. Oceanol. Limnol., 26: 276–279.
Kang J W. 1966. On the geographical distribution of marine algae in Korea. Bull. Pusan Fish. Coll., 7: 1–125.
Koh C H, Oh S H. 1992. Distribution pattern of macroalgae in the eastern Yellow Sea, Korean. Korean J. Phycol., 7: 139–146.
Larkin M. A, Blackshields G, Brown N P, Chenna R, McGettigan P A, McWilliam H, Valentin F, Wallace I M, Wilm A, Lopez R, Thompson J D, Gibson T J, Higgins D G. 2007. Clustal W and Clustal X version 2.0. Bioinformatics, 23: 2 947–2 948.
Lee H B, Lee I K. 1981. Flora of benthic marine algae in Gyeongi Bay, western coast of Korea. Korean J. Bot., 24: 107–138.
Lee I K, Lee Y D, Ahn Y S. 1986. Flora of marine algae in Cheju Island. I. Ulvaceae. Korean J. Bot., 1: 157–167.
Leskinen E, Pamilo P. 1997. Evolution of the ITS sequences of ribosomal DNA in Enteromorpha (Chlorophyceae). Hereditas, 126: 17–23.
Leskinen E, Alström-Rapaport C, Pamilo P. 2004. Phylogeographical structure, distribution and genetic variation of the green algae Ulva intestinalis and U. compressa (Chlorophyta) in the Baltic Sea area. Mol. Ecol., 13: 2 257–2 265.
Lie H J, Cho C H, Lee J H, Lee S, Tang Y. 2000. Seasonal variation of the Cheju Warm Current in the northern East China Sea. J. Oceanogr., 56: 197–211.
Loughnane C J, McIvor L M, Rindi F, Stengel D B, Guiry M D. 2008. Morphology, rbcL phylogeny and distribution of distromatic Ulva (Ulvophyceae, Chlorophyta) in Ireland and southern Britain. Phycologia, 47: 416–429.
Malta E J, Draisma S, Kamermans P. 1999. Free-floating Ulva in the southwest Netherlands: species or morphotypes? A morphological, molecular and ecological comparison. Eur. J. Phycol., 34: 443–454.
Manhart J R. 1994. Phylogenetic analysis of green plant rbcL sequences. Mol. Phylogenet. Evol., 3: 114–127.
Raffaelli D G, Raven J A, Poole L J. 1998. Ecological impact of green macroalgal blooms. Oceanogr. Mar. Biol., 36: 97–125.
Ronquist F, Huelsenbeck J P. 2003. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics, 19: 1 572–1 574.
Schories D, Reise K. 1993. Germination and anchorage of Enteromorpha spp. in sediments of the Wadden Sea. Helg. Meer., 47: 275–285.
Shimada S, Hiraoka M, Nabata S, Lima M, Masuda M. 2003. Molecular phylogenetic analyses of the Japanese Ulva and Enteromorpha (Ulvales, Ulvophyceae), with special reference to the free-floating Ulva. Phycol. Res., 51: 99–108.
Shimada S, Yokoyama N, Arai S, Hiraoka M. 2008. Phylogeography of the genus Ulva (Ulvophyceae, Chlorophyta), with special reference to the Japanese freshwater and brackish taxa. J. Appl. Phycol., 20: 979–989.
Stamatakis A. 2006. RAxML-VI-HPC: Maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics, 22: 2 688–2 690.
Sun S, Wang F, Li C, Qin S, Zhou M, Ding L, Pang S, Duan D, Wang G, Yin B, Yu R, Jiang P, Liu Z, Zhang G, Fei X, Zhou M. 2008. Emerging challenges: Massive green algae blooms in the Yellow Sea. Nat. prec., hdl: 10101/npre. 2008. 2266. 1.
Swofford D L. 2002. PAUP*. phylogenetic analysis using parsimony (and other methods) 4.0 beta. Sinauer Associates, Sunderland, USA.
Tan I H, Blomster J, Hansen G, Leskinen E, Maggs C A, Mann D G, Sluiman H J, Stanhope M J. 1999. Molecular phylogenetic evidence for a reversible morphogenetic switch controlling the gross morphology of two common genera of green seaweeds, Ulva and Enteromorpha. Mol. Biol. Evol., 16: 1 011–1 018.
Tseng C K, Chang C F. 1963. A preliminary analytical study of the Chinese marine algal flora. Oceanol. et Limnol. Sin., 5: 245–252. (in Chinese)
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.
van den Hoek C, Mann D G, Jahns H M. 1995. Algae. An Introduction to Phycology. Cambridge University Press, Cambridge, UK.
Wang J, Jiang P, Cui Y, Li N, Wang M, Lin H, He P, Qin S. 2010. Molecular analysis of green-tide-forming macroalgae in the Yellow Sea. Aqua. Bot., 93: 25–31.
Yoon M Y, Boo S. M. 1991. Flora and zonation of marine plants at the littoral area of Sapsido Island on the Yellow Sea of Korea. Korean. J. Phycol., 6: 145–156.
Yoshida T. 1998. Marine Algae of Japan. Uchida Rokakuho Press, Tokyo, Japan. p. 1 222. (in Japanese)
Author information
Authors and Affiliations
Corresponding authors
Additional information
Supported by the National Key Technology Research and Development Program (No. 2008BAC49B01), National High Technology Research and Development Program of China (863 Program) (No. 2009AA10Z106) and the Knowledge Innovation Project of the Chinese Academy of Sciences (No. KZCX2-YW-209)
Rights and permissions
About this article
Cite this article
Wang, J., Li, N., Jiang, P. et al. Ulva and Enteromorpha (Ulvaceae, Chlorophyta) from two sides of the Yellow Sea: analysis of nuclear rDNA ITS and plastid rbcL sequence data. Chin. J. Ocean. Limnol. 28, 762–768 (2010). https://doi.org/10.1007/s00343-010-9069-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00343-010-9069-3