Cite this paper:
Qingchun ZHANG, Zhuang NIU, Jinxiu WANG, Chao LIU, Fanzhou KONG, Xiaokun HU, Jiayu ZHAO, Rencheng YU. Development of high-resolution chloroplast markers for intraspecific phylogeographic studies of Phaeocystis globosa[J]. Journal of Oceanology and Limnology, 2021, 39(2): 508-524

Development of high-resolution chloroplast markers for intraspecific phylogeographic studies of Phaeocystis globosa

Qingchun ZHANG1,2,3, Zhuang NIU1,2,3,4, Jinxiu WANG1,2,3,4, Chao LIU1,2,3,4, Fanzhou KONG1,2,3, Xiaokun HU1,2,3,4, Jiayu ZHAO1,2,3,4, Rencheng YU1,2,3,4
1 CAS Key Laboratory of Marine Ecology and Environmental Sciences, Institute of Oceanology, Chinese Academy of Sciences, Qingdao 266071, China;
2 Laboratory for Marine Ecology and Environmental Sciences, Pilot National Laboratory for Marine Science and Technology (Qingdao), Qingdao 266237, China;
3 Center of Ocean Mega-Science, Chinese Academy of Sciences, Qingdao 266071, China;
4 University of Chinese Academy of Sciences, Beijing 100049, China
Abstract:
Phaeocystis globosa is an important harmful algal bloom causative species distributing widely in temperate and tropical coastal waters in the world. The morphological, physiological, and biochemical characteristics are different among geographic strains, which can not be distinguished with nuclear ribosomal DNA markers at present. Therefore, the genetic distance and phylogeographic relationships of nuclear 28S rDNA D1-D2 and ITS regions, and three chloroplast intergenic spacers (petN-trnS1, trnM1-psbA, and rbcS-rpl27) were analyzed and compared among 13 strains of P. globosa isolated from the Pacific Ocean and Atlantic Ocean in this study. In addition, the nucleotide polymorphisms of 28S rDNA D1-D2, ITS, and rbcS-rpl27 regions were evaluated in two P. globosa strains. The various levels of nucleotide polymorphism were in the nuclear 28S rDNA D1-D2 region and ITS region, but no polymorphism was in the chloroplast rbcS-rpl27 intergenic spacer. A reasonable intraspecific phylogeographic relationship was presented by rbcS-rpl27 intergenic spacer, which had the strongest distinction to geographic strains compared to those of 28S rDNA D1-D2 and ITS regions. In the phylogenetic tree of rbcS-rpl27 intergenic spacer, the two strains from the North Sea of the Atlantic Ocean were divided firstly from the species of P. globosa, and then formed an independent clade, while the other Atlantic strains and all of Pacific strains joined up to build the other clade. It was implied that at least two genetically distant populations of P. globosa existed in the Atlantic coastal regions. This study provided a high-resolution chloroplast marker to analyze intraspecific phylogeographic populations of P. globosa, and preliminarily clarified the genetic relationships of the Pacific and Atlantic strains of P. globosa.
Key words:    Phaeocystis globosa|chloroplast|DNA marker|phylogeny   
Received: 2019-11-18   Revised: 2020-01-23
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Articles by Qingchun ZHANG
Articles by Zhuang NIU
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Articles by Jiayu ZHAO
Articles by Rencheng YU
References:
Antajan E, Chrétiennot-Dinet M J, Leblanc C, Daro M H, Lancelot C. 2004. 19'-hexanoyloxyfucoxanthin may not be the appropriate pigment to trace occurrence and fate of Phaeocystis:the case of P. globosa in Belgian coastal waters. Journal of Sea Research, 52(3):165-177.
Bakker F T, Culham A, Daugherty L C, Gibby M. 1999. A trnL-F based phylogeny for species of Pelargonium(Geraniaceae) with small chromosomes. Plant Systematics and Evolution, 216(3-4):309-324.
Blomster J, Maggs C A, Stanhope M J. 1998. Molecular and morphological analysis of Enteromorpha intestinalis and E. compressa (Chlorophyta) in the British Isles. Journal of Phycology, 34(2):319-340.
Cadée G C. 1996. Accumulation and sedimentation of Phaeocystis globosa in the Dutch Wadden Sea. Journal of Sea Research, 36(3-4):321-327.
Carbonell-Caballero J, Alonso R, Ibañez V, Terol J, Talon M, Dopazo J. 2015. A phylogenetic analysis of 34 chloroplast genomes elucidates the relationships between wild and domestic species within the genus Citrus. Molecular Biology and Evolution, 32(8):2 015-2 035.
Charlson R J, Lovelock J E, Andreae M O, Warren S G. 1987. Oceanic phytoplankton, atmospheric sulphur, cloud albedo and climate. Nature, 326(6114):655-661.
Chen Y Q, Shao P, Wang N, Zhou H, Qu L H, Medlin L K. 2003. Molecular identification of bloom-forming species Phaeocystis globosa (Prymnesiophyta) and its dispersal based on rDNA ITS sequence analysis. Acta Oceanologica Sinica, 22(2):243-253.
Chen Y Q, Wang N, Zhang P, Zhou H, Qu L H. 2002. Molecular evidence identifies bloom-forming Phaeocystis(Prymnesiophyta) from coastal waters of southeast China as Phaeocystis globosa. Biochemical Systematics and Ecology, 30(1):15-22.
Crooks G E, Hon G, Chandonia J M, Brenner S E. 2004. WebLogo:a sequence logo generator. Genome Research, 14:1 188-1 190.
Darling K F, Kucera M, Pudsey C J, Wade C M. 2004. Molecular evidence links cryptic diversification in polar planktonic protists to quaternary climate dynamics. Proceedings of the National Academy of Sciences of the United States of America, 101(20):7 657-7 662.
Darling K F, Wade C M, Stewart I A, Kroon D, Dingle R, Brown A J L. 2000. Molecular evidence for genetic mixing of Arctic and Antarctic subpolar populations of planktonic foraminifers. Nature, 405(6782):43-47.
Davidson A T, Marchant H I. 1992. The biology and ecology of Phaeocystis (Prymnesiophyceae). In:Round F E eds. Progress in Phycological Research. Biopress, Bristol. p.1-45.
Decelle J, Probert I, Bittner L, Desdevises Y, Colin S, de Vargas C, Gali M, Simó R, Not F. 2012. An original mode of symbiosis in open ocean plankton. Proceedings of the National Academy of Sciences of the United States of America, 109(44):18 000-18 005.
Hai D N, Lam N N, Dippner J W. 2010. Development of Phaeocystis globosa blooms in the upwelling waters of the south central coast of Viet Nam. Journal of Marine Systems, 83(3-4):253-261.
Hu X K, Zhang Q C, Chen Z F, Kong F Z, Wang J X, Yu R C. 2019a. Genetic diversity of Phaeocystis globosa strains isolated from the Beihu Gulf, the South China Sea. Oceanologia et Limnologia Sinica, 50(3):601-609. (in Chinese with English abstract)
Hu Z M, Uwai S, Yu S H, Komatsu T, Ajisaka T, Duan D L. 2011. Phylogeographic heterogeneity of the brown macroalga Sargassum horneri (Fucaceae) in the northwestern Pacific in relation to late Pleistocene glaciation and tectonic configurations. Molecular Ecology, 20(18):3 894-3 909.
Hu Z X, Deng Y Y, Tang Y Z. 2019b. Scanning and transmission electron microscopy observation on morphology and ultrastructure of Phaeocystis globosa from Beibu Gulf, China. Oceanologia et Limnologia Sinica, 50(3):621-629. (in Chinese with English abstract)
Jacobsen A. 2002. Morphology, relative DNA content and hypothetical life cycle of Phaeocystis pouchetii(Prymnesiophyceae); with special emphasis on the flagellated cell type. Sarsia, 87(5):338-349.
Kalyaanamoorthy S, Minh B Q, Wong T K F, von Haeseler A, Jermiin L S. 2017. ModelFinder:fast model selection for accurate phylogenetic estimates. Nature Methods, 14(6):587-589.
Katayama H, Tachibana M, Iketani H, Zhang S L, Uematsu C. 2012. Phylogenetic utility of structural alterations found in the chloroplast genome of pear:hypervariable regions in a highly conserved genome. Tree Genetics & Genomes, 8(2):313-326.
Kholina A B, Kozyrenko M M, Artyukova E V, Sandanov D V, Andrianova E A. 2016. Phylogenetic relationships of the species of Oxytropis DC. subg. Oxytropis and Phacoxytropis (Fabaceae) from Asian Russia inferred from the nucleotide sequence analysis of the intergenic spacers of the chloroplast genome. Russian Journal of Genetics, 52(8):780-793.
Kimura T, Iketani H, Kotobuki K, Matsuta N, Ban Y, Hayashi T, Yamamoto T. 2003. Genetic characterization of pear varieties revealed by chloroplast DNA sequences. Journal of Horticultural Science and Biotechnology, 78(2):241-247.
Kumar S, Stecher G, Li M, Knyaz C, Tamura K. 2018. MEGA X:molecular evolutionary genetics analysis across computing platforms. Molecular Biology and Evolution, 35(6):1 547-1 549.
Lancelot C, Billen G, Sournia A, Weisse T, Colijn F, Veldhuis M J W, Davies A, Wassman P. 1987. Phaeocystis blooms and nutrient enrichment in the continental coastal zones of the North Sea. Ambio, 16(1):38-46.
Lange M, Chen Y Q, Medlin L K. 2002. Molecular genetic delineation of Phaeocystis species (Prymnesiophyceae) using coding and non-coding regions of nuclear and plastid genomes. European Journal of Phycology, 37(1):77-92.
Li P R, Zhang S J, Li F, Zhang S F, Zhang H, Wang X W, Sun R F, Bonnema G, Borm T J A. 2017. A phylogenetic analysis of chloroplast genomes elucidates the relationships of the six economically important Brassica species comprising the triangle of U. Frontiers in Plant Science, 8:111, https://doi.org/10.3389/fpls.2017.00111.
Liss P S, Malin G, Turner S M, Holligan P M. 1994. Dimethyl sulphide and Phaeocystis:a review. Journal of Marine Systems, 5(1):41-53.
Liu H L, Zhang Q, Jiang Q M, Ma B. 2010. Analyses of sequence variation and secondary structure on rDNA ITS regions of the strains of redtide-caused harmful algae Phaeocystis globosa. Ecological Science, 29(5):432-437.(in Chinese with English abstract)
Liu J S, Peng X C, Yang W D. 2007. AFM observation of hemolytic extracts from Phaeocystis globosa on rabbit erythrocytes. Journal of Tropical Oceanography, 26(2):55-58. (in Chinese with English abstract)
Medlin L, Zingone A. 2007. A taxonomic review of the genus Phaeocystis. Biogeochemistry, 83(1-3):3-18.
Paul H A, Zachos J C, Flower B P, Tripati A. 2000. Orbitally induced climate and geochemical variability across the Oligocene/Miocene boundary. Paleoceanography, 15(5):471-485.
Peperzak L, Colijn F, Vrieling E G, Gieskes W W C, Peeters J C H. 2000. Observations of flagellates in colonies of Phaeocystis globosa (Prymnesiophyceae); a hypothesis for their position in the life cycle. Journal of Plankton Research, 22(12):2 181-2 203.
Peperzak L, Gäbler-Schwarz S. 2012. Current knowledge of the life cycles of Phaeocystis globosa and Phaeocystis antarctica (Prymnesiophyceae). Journal of Phycology, 48(3):514-517.
Qi Y Z, Chen J F, Wang Z H, Xu N, Wang Y, Shen P P, Lu S H, Hodgkiss I J. 2004. Some observations on harmful algal bloom (HAB) events along the coast of Guangdong, southern China in 1998. Hydrobiologia, 512(1-3):209-214.
Qu L Y, Lv S H, Gao C L, Li Y, Sun P, Sun X Q. 2008. Structure and sequence analysis of 18s rDNA and ITS gene of Phaeocystis isolate from the Bohai Sea. Advances in Marine Science, 26(2):200-206. (in Chinese with English abstract)
Raman G, Choi K S, Park S. 2016. Phylogenetic relationships of the fern Cyrtomium falcatum (Dryopteridaceae) from Dokdo Island based on chloroplast genome sequencing. Genes, 7(12):115.
Ronquist F, Teslenko M, van der Mark P, Ayres D L, Darling A, Höhna S, Larget B, Liu L, Suchard M A, Huelsenbeck J P. 2012. MrBayes 3.2:efficient Bayesian phylogenetic inference and model choice across a large model space. System Biology, 61(3):539-542.
Rousseau V, Chrétiennot-Dinet M J, Jacobsen A, Verity P, Whipple S. 2007. The life cycle of Phaeocystis:state of knowledge and presumptive role in ecology. Biogeochemistry, 83(1-3):29-47.
Rousseau V, Lantoine F, Rodriguez F, LeGall F, ChrétiennotDinet M J, Lancelot C. 2013. Characterization of Phaeocystis globosa (Prymnesiophyceae), the blooming species in the Southern North Sea. Journal of Sea Research, 76:105-113.
Rousseau V, Vaulot D, Casotti R, Cariou V, Lenz J, Gunkel J, Baumann M. 1994. The life cycle of Phaeocystis(Prymnesiophycaea):evidence and hypotheses. Journal of Marine Systems, 5(1):23-39.
Schoemann V, Becquevort S, Stefels J, Rousseau V, Lancelot C. 2005. Phaeocystis blooms in the global ocean and their controlling mechanisms:a review. Journal of Sea Research, 53(1-2):43-66.
Seoane S, Zapata M, Orive E. 2009. Growth rates and pigment patterns of haptophytes isolated from estuarine waters. Journal of Sea Research, 62(4):286-294.
Shen P, Van Rijssel M, Wang Y, Lu S H, Chen J F, Qi Y Z. 2004. Toxic Phaeocystis globosa strains from China grow at remarkably high temperatures. In:Steidinger K A, Landsberg J H, Tomas C R, Vargo G A eds. Harmful Algae 2002. Florida Fish and Wildlife Conservation Commission, Florida Institute of Oceanography and Intergovernmental Oceanographic Commission of UNESCO, St. Petersburg. p.396-398.
Shi M C, Chen C S, Xu Q C, Lin H C, Liu G M, Wang H, Wang F, Yan J H. 2002. The role of Qiongzhou Strait in the seasonal variation of the South China Sea circulation. Journal of Physical Oceanography, 32(1):103-121.
Smith D R, Arrigo K R, Alderkamp A C, Allen A E. 2014a. Massive difference in synonymous substitution rates among mitochondrial, plastid, and nuclear genes of Phaeocystis algae. Molecular Phylogenetics and Evolution, 71:36-40.
Smith W O Jr, Liu X, Tang K W, DeLizo L M, Doan N H, Nguyen N L, Wang X D. 2014b. Giantism and its role in the harmful algal bloom species Phaeocystis globosa. Deep Sea Research Part II:Topical Studies in Oceanography, 101:95-106.
Stefels J, Dijkhuizen L, Gieskes W W C. 1995. DMSP-lyase activity in a spring phytoplankton bloom off the Dutch coast, related to Phaeocystis sp. abundance. Marine Ecology Progress Series, 123:235-243.
Stefels J, Van Boekel W H M. 1993. Production of DMS from dissolved DMSP in axenic cultures of the marine phytoplankton species Phaeocystis sp. Marine Ecology Progress Series, 97:11-18.
Vaulot D, Birrien J L, Marie D, Casotti R, Veldhuis M J W, Kraay G W, Chrétiennot-Dinet M J. 1994. Morphology, ploidy, pigment composition, and genome size of cultured strains of Phaeocystis (Prymnesiophyceae). Journal of Phycology, 30(6):1 022-1 035.
Vitales D, Aragay J, Garnatje T, Garreta A G, Lluch J R. 2019. Phylogeography of Dictyota fasciola and Dictyota mediterranea (Dictyotales, Phaeophyceae):unexpected patterns on the Atlantic-Mediterranean marine transition and taxonomic implications. PeerJ, 7(6):e6916, https://doi.org/10.7717/peerj.6916.
Wang J X, Kong F Z, Chen Z F, Zhang Q C, Yu R C, Zhou M J. 2019. Characterization of pigment composition of six strains of Phaeocystis globosa. Oceanologia et Limnologia Sinica, 50(3):611-620. (in Chinese with English abstract)
Wassmann P, Ratkova T, Reigstad M. 2005. The contribution of single and colonial cells of Phaeocystis pouchetii to spring and summer blooms in the north-eastern North Atlantic. Harmful Algae, 4(5):823-840.
Whipple S J, Patten B C, Verity P G. 2005a. Colony growth and evidence for colony multiplication in Phaeocystis pouchetii (Prymnesiophyceae) isolated from mesocosm blooms. Journal of Plankton Research, 27(5):495-501.
Whipple S J, Patten B C, Verity P G. 2005b. Life cycle of the marine alga Phaeocystis:a conceptual model to summarize literature and guide research. Journal of Marine Systems, 57(1-2):83-110.
Winnepenninckx B, Backeljau T, De Wachter R. 1993. Extraction of high molecular weight DNA from mollusks. Trends in Genetics, 9(12):407.
Wolfe K H, Li W H, Sharp P M. 1987. Rates of nucleotide substitution vary greatly among plant mitochondrial, chloroplast, and nuclear DNAs. Proceedings of the National Academy of Sciences of the United States of America, 84(24):9 054-9 058.
Yan H D, Zhang X Q, Fu C, Huang L K, Yin G H, Nie G, Xu W Z, Liu X C, Chen T, Lee S, Ma X, Peng Y, Yan Y H, Ling Y, Liu W. 2015. Chloroplast DNA variation and genetic structure of Miscanthus sinensis in southwest China. Biochemical Systematics and Ecology, 58:132-138.
Yang Q C, Chen L N, Hu X L, Zhao L, Yin P H, Li Q. 2015. Toxic effect of a marine bacterium on aquatic organisms and its algicidal substances against Phaeocystis globosa. PLoS One, 10(2):e0114933, https://doi.org/10.1371/journal.pone.0114933.
Yang Z M, Zhang Q, Xie S T, Han B P, Lv S H, Hodgkiss I J. 2004. Sequence analyses of chloroplastic psaA gene fragment from Phaeocystis globosa. Journal of Tropical and Subtropical Botany, 12(5):435-439. (in Chinese with English abstract)
Zapata M, Jeffrey S W, Wright S W, Rodríguez F, Garrido J L, Clementson L. 2004. Photosynthetic pigments in 37 species (65 strains) of Haptophyta:implications for oceanography and chemotaxonomy. Marine Ecology Progress Series, 270:83-102.
Zhang J, Huang X, Huang D J, Zhang Y, Huang L K, Lu L, Yan H D. 2016. Studies on genetic diversity and phylogenetic relationships of limpograss (Hemarthria altissima) and related species based on combined chloroplast DNA intergenic spacer data. Biochemical Systematics and Ecology, 69:91-100.
Zhou T, Ruhsam M, Wang J, Zhu H H, Li W L, Zhang X, Xu Y C, Xu F S, Wang X M. 2019. The complete chloroplast genome of Euphrasia regelii, pseudogenization of ndh genes and the phylogenetic relationships within Orobanchaceae. Frontiers in Genetics, 10:444, https://doi.org/10.3389/fgene.2019.00444.
Zingone A, Chrétiennot-Dinet M J, Lange M, Medlin L. 1999. Morphological and genetic characterization of Phaeocystis cordata and P. jahnii (Prymnesiophyceae), two new species from the Mediterranean Sea. Journal of Phycology, 35(6):1 322-1 337.
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