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An appraisal of Ulva (Ulvophyceae, Chlorophyta) taxonomy

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Abstract

The green seaweed Ulva is important from ecological and economic perspectives, but the identification of species is often problematic. Here we assessed and discussed different perspectives to establish a stable taxonomic framework for Ulva, which will benefit both ecological and applied research. We evaluated (1) the performance of commonly used DNA-barcode markers (ITS rDNA, rbcL, and tufA) using species delimitation methods (PTP and GMYC), (2) the usage of species names in the literature, and (3) the geographic coverage of genetic data to identify poorly sampled regions. Species delimitation employing the tufA gene was the most consistent across methods. Not surprisingly, DNA-based species delimitation was often in disagreement with traditional morphology-based species definitions. Biological species concepts, where tested, proved to be generally narrower than DNA-based species delimitation. Although the use of molecular markers has greatly improved our view of Ulva diversity, the names associated with DNA sequences in public databases are often unreliable, complicating species identification. Recently, sequencing type materials has considerably reduced the gap between DNA sequence data and Linnaean names, but our knowledge on Ulva diversity remains inadequate, especially in tropical regions. Perspectives for Ulva taxonomy include the consistent use of multiple DNA-barcode markers assisted by species delimitation methods, applications of genomic data, and crossing experiments. To arrive at a stable nomenclature, we outline the benefits and shortcomings of adhering to the rules and practices of the International Code of Nomenclature for algae, fungi, and plants, for example, by sequencing name-bearing types and discuss alternative approaches.

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Data availability

The authors declare that the data supporting the findings of this study are available within the article, its supplementary information files, and on the open-access repository Zenodo (https://zenodo.org/record/5816815).

References

  • Ahrens D, Fujisawa T, Krammer H-J, Eberle J, Fabrizi S, Vogler AP (2016) Rarity and incomplete sampling in DNA-based species delimitation. Syst Biol 65:478–494

    Article  PubMed  Google Scholar 

  • Anisimova M, Gascuel O (2006) Approximate likelihood-ratio test for branches: A fast, accurate, and powerful alternative. Syst Biol 55:539–552

    Article  PubMed  Google Scholar 

  • Ashkenazi DY, Israel A, Abelson A (2019) A novel two-stage seaweed integrated multi-trophic aquaculture. Rev Aquacult 11:246–262

    Article  Google Scholar 

  • Bast F, Rani P (2019) First report of uniseriate free-living Ulva species with description of new species Ulva uniseriata sp. nov. (Chlorophyta, Ulvales). Indian J Mar Sci 48(11):1687–1691

  • Bergsten J, Bilton DT, Fujisawa T, Elliott M, Monaghan MT, Balke M, Hendrich L, Geijer J, Herrmann J, Foster GN, Ribera I, Nilsson AN, Barraclough TG, Vogler AP (2012) The effect of geographical scale of sampling on DNA barcoding. Syst Biol 61:851–869

    Article  PubMed  PubMed Central  Google Scholar 

  • Bliding C (1968) A critical survey of European taxa Ulvales Part II. Ulva, Ulvaria, Monostroma, Kornmannia. Bot Not 121:535–629

    Google Scholar 

  • Bliding C (1963) A critical survey of European taxa in Ulvales. Part I. Capsosiphon, Percursaria, Blidingia, Enteromorpha. Opera Bot 8 (3):1–160

  • Blomster J, Maggs CA, Stanhope MJ (1999) Extensive intraspecific morphological variation in Enteromorpha muscoides (Chlorophyta) revealed by molecular analysis. J Phycol 35:575–586

    Article  Google Scholar 

  • Bunning SL, Jones G, Brown TA (2012) Next generation sequencing of DNA in 3300-year-old charred cereal grains. J Archaeol Sci 39:2780–2784

    Article  CAS  Google Scholar 

  • Charrier B, Abreu MH, Araujo R, Bruhn A, Coates JC, De Clerck O, Katsaros C, Robaina RR, Wichard T (2017) Furthering knowledge of seaweed growth and development to facilitate sustainable aquaculture. New Phytol 216:967–975

    Article  PubMed  Google Scholar 

  • Chen L, Feng J, Xie S-l (2015) Ulva shanxiensis (Ulvaceae), a new species from Shanxi. China. Novon 23(4):397–405

  • Cui J, Monotilla AP, Zhu W, Takano Y, Shimada S, Ichihara K, Matsui T, He P, Hiraoka M (2018) Taxonomic reassessment of Ulva prolifera (Ulvophyceae, Chlorophyta) based on specimens from the type locality and Yellow Sea green tides. Phycologia 57:692–704

    Article  CAS  Google Scholar 

  • De Clerck O, Guiry MD, Leliaert F, Samyn Y, Verbruggen H (2013) Algal taxonomy: a road to nowhere? J Phycol 49:215–225

    Article  PubMed  Google Scholar 

  • De Clerck O, Kao S-M, Bogaert KA, Blomme J, Foflonker F, Kwantes M, Vancaester E, Vanderstraeten L, Aydogdu E, Boesger J, Califano G, Charrier B, Clewes R, Del Cortona A, D’Hondt S, Fernandez-Pozo N, Gachon CM, Hanikenne M, Lattermann L, Leliaert F, Liu X, Maggs CA, Popper ZA, Raven JA, Van Bel M, Wilhelmsson PKI, Bhattacharya D, Coates JC, Rensing SA, Van Der Straeten D, Vardi A, Sterck L, Vandepoele K, Van de Peer Y, Wichard T, Bothwell JH (2018) Insights into the evolution of multicellularity from the sea lettuce genome. Curr Biol 28:2921-2933.e2925

    Article  CAS  PubMed  Google Scholar 

  • Drummond AJ, Rambaut A (2007) BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol 7:214

    Article  PubMed  PubMed Central  Google Scholar 

  • Ezard T, Fujisawa T, Barraclough TG (2009) Splits: species’ limits by threshold statistics. R package version 1019

  • Forin N, Nigris S, Voyron S, Girlanda M, Vizzini A, Casadoro G, Baldan B (2018) Next generation sequencing of ancient fungal specimens: The case of the Saccardo Mycological Herbarium. Front Ecol Evol 6:129

    Article  Google Scholar 

  • Fort A, Mannion C, Fariñas-Franco JM, Sulpice R (2020a) Green tides select for fast expanding Ulva strains. Sci Total Environ 698:134337

    Article  CAS  PubMed  Google Scholar 

  • Fort A, McHale M, Cascella K, Potin P, Usadel B, Guiry MD, Sulpice R (2020b) Foliose Ulva species show considerable inter-specific genetic diversity, low intra-specific genetic variation, and the rare occurrence of inter-specific hybrids in the wild. J Phycol 57:219–233

    Article  PubMed  PubMed Central  Google Scholar 

  • Fort A, McHale M, Cascella K, Potin P, Perrineau MM, Kerrison PD, da Costa E, Calado R, Domingues MDR, Costa Azevedo I, Sousa-Pinto I, Gachon C, van der Werf A, de Visser W, Beniers JE, Jansen H, Guiry MD, Sulpice R (2022) Exhaustive reanalysis of barcode sequences from public repositories highlights ongoing misidentifications and impacts taxa diversity and distribution. Mol Ecol Resour 22:86–101

    Article  CAS  PubMed  Google Scholar 

  • Føyn B (1955) Specific differences between northern and southern European populations of the green alga Ulva lactuca L. Pubbl Stn Zool Napoli 27:261–270

    Google Scholar 

  • Fujisawa T, Barraclough TG (2013) Delimiting species using single-locus data and the Generalized Mixed Yule Coalescent approach: A revised method and evaluation on simulated data sets. Syst Biol 62:707–724

    Article  PubMed  PubMed Central  Google Scholar 

  • Guidone M, Thornber C, Wysor B, O’Kelly CJ (2013) Molecular and morphological diversity of Narragansett Bay (RI, USA) Ulva (Ulvales, Chlorophyta) populations. J Phycol 49:979–995

    Article  CAS  PubMed  Google Scholar 

  • Guindon S, Dufayard J-F, Lefort V, Anisimova M, Hordijk W, Gascuel O (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: Assessing the performance of PhyML 3.0. Syst Biol 59:307–321

  • Guiry MD, Guiry GM (2021) AlgaeBase. World-wide electronic publication. National University of Ireland, Galway. http://www.algaebase.org. Accessed 6 Jan 2021

  • Hanyuda T, Kawai H (2018) Genetic examination of the type specimen of Ulva australis suggests that it was introduced to Australia. Phycol Res 66:238–241

    Article  CAS  Google Scholar 

  • Hardisty A, Saarenmaa H, Casino A, Dillen M, Gödderz K, Groom Q, Hardy H, Koureas D, Nieva de la Hidalga A, Paul DL, Runnel V, Vermeersch X, van Walsum M, Willemse L (2020) Conceptual design blueprint for the DiSSCo digitization infrastructure - DELIVERABLE D8.1. Research Ideas and Outcomes 6:e54280

  • Hayden HS, Waaland JR (2004) A molecular systematic study of Ulva (Ulvaceae, Ulvales) from the northeast Pacific. Phycologia 43:364–382

    Article  Google Scholar 

  • Hayden HS, Blomster J, Maggs CA, Silva PC, Stanhope MJ, Waaland JR (2003) Linnaeus was right all along: Ulva and Enteromorpha are not distinct genera. Eur J Phycol 38:277–294

    Article  Google Scholar 

  • He Y, Shen S, Yu D, Wang Y, Yin J, Wang Z, Ye Y (2021) The Ulva prolifera genome reveals the mechanism of green tides. J Oceanol Limnol 39:1458–1470

  • Heesch S, Broom JES, Neill KF, Farr TJ, Dalen JL, Nelson WA (2009) Ulva, Umbraulva and Gemina: genetic survey of New Zealand taxa reveals diversity and introduced species. Eur J Phycol 44:143–154

    Article  CAS  Google Scholar 

  • Hiraoka M, Enomoto S (1998) The induction of reproductive cell formation of Ulva pertusa Kjellman (Ulvales, Ulvophyceae). Phycol Res 46:199–203

    Article  Google Scholar 

  • Hiraoka M, Ichihara K, Zhu W, Shimada S, Oka N, Cui J, Tsubaki S, He P (2017) Examination of species delimitation of ambiguous DNA-based Ulva (Ulvophyceae, Chlorophyta) clades by culturing and hybridisation. Phycologia 56:517–532

    Article  CAS  Google Scholar 

  • Hiraoka M, Shimada S, Ohno M, Serisawa Y (2003) Asexual life history by quadriflagellate swarmers of Ulva spinulosa (Ulvales, Ulvophyceae). Phycol Res 51:29–34

  • Hiraoka M, Shimada S, Uenosono M, Masuda M (2004) A new green-tide-forming alga, Ulva ohnoi Hiraoka et Shimada sp. nov. (Ulvales, Ulvophyceae) from Japan. Phycol Res 52:17–29

  • Hoeksema BW, van den Hoek C (1983) The taxonomy of Ulva (Chlorophyceae) from the coastal region of Roscoff (Brittany, France). Bot Mar 26:65–86

  • Horimoto R, Masakiyo Y, Ichihara K, Shimada S (2011) Enteromorpha-like Ulva (Ulvophyceae, Chlorophyta) growing in the Todoroki River, Ishigaki Island, Japan, with species reference to Ulva meridionalis Horimoto et Shimada sp. nov. Kokuritsu Kagaku Hakubutsukan Kenkyu Hokoku (B-rui). Bull Nat 37:155–167

  • Huang Y, Niu B, Gao Y, Fu L, Li W (2010) CD-HIT Suite: a web server for clustering and comparing biological sequences. Bioinformatics (Oxford) 26:680–682

  • Huisman JM (ed) (2015) Algae of Australia: marine benthic algae of north-western Australia. 1. Green and brown algae. Australian Biological Resources Study & CSIRO Publishing, Canberra & Melbourne 

  • Hughey JR, Miller KA, Gabrielson PW (2018) Mitogenome analysis of a green tide forming Ulva from California, USA confirms its identity as Ulva expansa (Ulvaceae, Chlorophyta). Mitochondrial DNA B 3:1302–1303

    Article  Google Scholar 

  • Hughey JR, Maggs CA, Mineur F, Jarvis C, Miller KA, Shabaka SH, Gabrielson PW (2019) Genetic analysis of the Linnaean Ulva lactuca (Ulvales, Chlorophyta) holotype and related type specimens reveals name misapplications, unexpected origins, and new synonymies. J Phycol 55:503–508

    Article  CAS  PubMed  Google Scholar 

  • Hughey JR, Gabrielson PW, Maggs CA, Mineur F (2022) Genomic analysis of the lectotype specimens of European Ulva rigida and Ulva lacinulata (Ulvaceae, Chlorophyta) reveals the ongoing misapplication of names. Eur J Phycol 57:143–153

  • Hughey JR, Gabrielson PW, Maggs CA, Mineur F, Miller KA (2020) Taxonomic revisions based on genetic analysis of type specimens of Ulva conglobata, U. laetevirens, U. pertusa and U. spathulata (Ulvales, Chlorophyta). Phycol Res 69:148–153

  • Ichihara K, Arai S, Uchimura M, Fay EJ, Ebata H, Hiraoka M, Shimada S (2009) New species of freshwater Ulva, Ulva limnetica (Ulvales, Ulvophyceae) from the Ryukyu Islands. Japan Phycol Res 57:94–103

    Article  Google Scholar 

  • Index Nominum Algarum (2021), University Herbarium, University of California, Berkeley. Compiled by Paul Silva. Available online at http://ucjeps.berkeley.edu/INA.html

  • Kalyaanamoorthy S, Minh BQ, Wong TKF, von Haeseler A, Jermiin LS (2017) ModelFinder: fast model selection for accurate phylogenetic estimates. Nat Meth 14:587–589

    Article  CAS  Google Scholar 

  • Kang JH, Jang JE, Kim JH, Byeon SY, Kim S, Choi SK, Kang YH, Park SR, Lee HJ (2019) Species composition, diversity, and distribution of the genus Ulva along the coast of Jeju Island, Korea based on molecular phylogenetic analysis. PLoS ONE 14:e0219958

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Katoh K, Standley DM (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 30:772–780

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kazi MA, Kavale MG, Singh VV (2016) Morphological and molecular characterization of Ulva chaugulii sp. nov., U. lactuca and U. ohnoi (Ulvophyceae, Chlorophyta) from India. Phycologia 55(1):45–54

  • Kiana P, Khosro P, Jelveh S, Saied Tamadoni J, Jaanika B (2016) Molecular and morphological characterisation of Ulva chaugulii, U. paschima and U. ohnoi (Ulvophyceae) from the Persian Gulf, Iran. Bot Mar 59:147–158

  • Kirkendale L, Saunders GW, Winberg P (2013) A molecular survey of Ulva (Chlorophyta) in temperate Australia reveals enhanced levels of cosmopolitanism. J Phycol 49:69–81

    Article  PubMed  Google Scholar 

  • Koeman RPT, van den Hoek C (1981) The taxonomy of Ulva (Chlorophyceae) in the Netherlands. Brit Phycol J 16:9–53

    Article  Google Scholar 

  • Kraft LGK, Kraft GT, Waller RF (2010) Investigations into Southern Australian Ulva (Ulvophyceae, Chlorophyta) taxonomy and molecular phylogeny indicate both cosmopolitanism and endemic cryptic species. J Phycol 46:1257–1277

    Article  Google Scholar 

  • Krupnik N, Paz GUY, Douek J, Lewinsohn E, Israel A, Carmel N, Mineur F, Maggs CA (2018) Native, invasive and cryptogenic Ulva species from the Israeli Mediterranean Sea: risk and potential. Medit Mar Sci 19:132–146

  • Larsen J (1981) Crossing experiments with Enteromorpha intestinalis and E. compressa from different European localities. Nord J Bot 1:128–136

  • Lee HW, Kang JC, Kim MS (2019) Taxonomy of Ulva causing blooms from Jeju Island, Korea with new species, U. pseudo-ohnoi sp. nov. (Ulvales, Chlorophyta). Algae 34:253–266

  • Lefort V, Longueville J-E, Gascuel O (2017) SMS: Smart model selection in PhyML. Mol Biol Evol 34:2422–2424

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Leliaert F, Verbruggen H, Vanormelingen P, Steen F, López-Bautista JM, Zuccarello GC, De Clerck O (2014) DNA-based species delimitation in algae. Eur J Phycol 49:179–196

    Article  Google Scholar 

  • Linnaeus C (1753) Species platarum, exhibentes plantas rite cognitas, ad genera relatas, cum differentiis specificus, nominibus trivialibus, synonymis selectis, locis natalibus, secundum systema sexuale digestas, vol 1 – 2. 1 edn., Salvii, Stockholm

  • Liu J, Zhao X, Kang X, Zhuang M, Ding X, Zhao L, Wen Q, Zhu Y, Gu K, Bao Q, Yang X, Zhang J, He P (2020) Good news: we can identify Ulva species erupted in the Yellow Sea more easily and cheaply now. Conserv Genet Resour 12:447–449

    Article  Google Scholar 

  • Liu J, Xia J, Zhuang M, Zhang J, Yu K, Zhao S, Sun Y, Tong Y, Xia L, Qin Y, He P, Liu W, Dai W, Xu H (2021) Controlling the source of green tides in the Yellow Sea: NaClO treatment of Ulva attached on Pyropia aquaculture rafts. Aquaculture 535:736378

    Article  CAS  Google Scholar 

  • Loughnane CJ, McIvor LM, Rindi F, Stengel DB, Guiry MD (2008) Morphology, rbcL phylogeny and distribution of distromatic Ulva (Ulvophyceae, Chlorophyta) in Ireland and southern Britain. Phycologia 47:416–429

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • Mantri VA, Kazi MA, Balar NB, Gupta V, Gajaria T (2020) Concise review of green algal genus Ulva Linnaeus. J Appl Phycol 32:2725–2741

    Article  Google Scholar 

  • Mares J, Leskinen E, Sitkowska M, Skacelova O, Blomster J (2011) True identity of the European freshwater Ulva (Chlorophyta, Ulvophyceae) revealed by a combined molecular and morphological approach. J Phycol 47:1177–1192

    Article  CAS  PubMed  Google Scholar 

  • Masakiyo Y, Shimada S (2014) Species diversity of the genus Ulva (Ulvophyceae, Chlorophyta) in Japanese waters, with special reference to Ulva tepida Masakiyo et S. Shimada sp. nov. Kokuritsu Kagaku Hakubutsukan Kenkyu Hokoku (B-rui)/Bull Nat 40:1–13

  • Matsumoto K, Shimada S (2015) Systematics of green algae resembling Ulva conglobata, with a description of Ulva adhaerens sp. nov. (Ulvales, Ulvophyceae). Eur J Phycol 50:100–111

  • Melton III JT, Lopez-Bautista JM (2021) Diversity of the green macroalgal genus Ulva (Ulvophyceae, Chlorophyta) from the east and gulf coast of the United States based on molecular data. J Phycol 57:551–568

    Article  Google Scholar 

  • Miller MA, Pfeiffer W, Schwartz T (2010) Creating the CIPRES Science Gateway for inference of large phylogenetic trees. In: 2010 Gateway Computing Environments Workshop, 14–14 Nov. 2010, pp 1–8

  • Mitsuhashi C, Teramura H, Shimada H (2020) Construction of genomic marker sets based on the chloroplast genome of a green alga, Ulva pertusa (syn. Ulva australis), leads to simple detection of Ulva species. Genes Genet Syst 95:55–63

  • Monotilla AP, Nishimura T, Adachi M, Tanii Y, Largo DB, Hiraoka M (2018) Examination of prezygotic and postzygotic isolating barriers in tropical Ulva (Ulvophyceae, Chlorophyta): evidence for ongoing speciation. J Phycol 54:539–549

    Article  CAS  PubMed  Google Scholar 

  • Neori A, Shpigel M, Ben-Ezra D (2000) A sustainable integrated system for culture of fish, seaweed and abalone. Aquaculture 186:279–291

    Article  Google Scholar 

  • Nguyen L-T, Schmidt HA, von Haeseler A, Minh BQ (2015) IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol Biol Evol 32:268–274

    Article  CAS  PubMed  Google Scholar 

  • O’Kelly CJ, Kurihara A, Shipley TC, Sherwood AR (2010) Molecular assessment of Ulva spp. (Ulvophyceae, Chlorophyta) in the Hawaiian islands. J Phycol 46:728–735

  • Ogawa T, Ohki K, Kamiya M (2013) Differences of spatial distribution and seasonal succession among Ulva species (Ulvophyceae) across salinity gradients. Phycologia 52:637–651

    Article  Google Scholar 

  • Page RDM (2016) DNA barcoding and taxonomy: dark taxa and dark texts. Phil Trans Roy Soc B 371:20150334

    Article  Google Scholar 

  • Prosser SW, deWaard JR, Miller SE, Hebert PD (2016) DNA barcodes from century-old type specimens using next-generation sequencing. Mol Ecol Resour 16:487–497

    Article  CAS  PubMed  Google Scholar 

  • R Core Team (2018) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. https://www.R-project.org

  • Rambaut A, Drummond AJ, Xie D, Baele G, Suchard MA (2018) Posterior summarization in Bayesian phylogenetics using Tracer 1.7. Syst Biol 67:901–904

  • Saunders GW, Kucera H (2010) An evaluation of rbcL, tufA, UPA, LSU and ITS as DNA barcode markers from the marine green macroalgae. Cryptogam Algol 31:487–528

    Google Scholar 

  • Sauriau P-G, Dartois M, Becquet V, Aubert F, Huet V, Bréret M, Viricel A, Pante E (2021) Multiple genetic marker analysis challenges the introduction history of Ulva australis (Ulvales, Chlorophyta) on French coasts. Eur J Phycol 56:455–467

    Article  Google Scholar 

  • Shimada S, Hiraoka M, Nabata S, Iima 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • Silva PC (1952) A review of nomenclatural conservation in the algae from the point of view of the type method. Univ Calif Publ Bot 25:241–324

    Google Scholar 

  • Škaloud P, Rindi F, Boedeker C, Leliaert F (2018) Freshwater flora of Central Europe, Vol 13: Chlorophyta: Ulvophyceae. Springer Spektrum, Berlin

  • Spalding HL, Conklin KY, Smith CM, O’Kelly CJ, Sherwood AR (2016) New Ulvaceae (Ulvophyceae, Chlorophyta) from mesophotic ecosystems across the Hawaiian Archipelago. J Phycol 52(1):40–53

    Article  PubMed  Google Scholar 

  • Steinhagen S, Barco A, Wichard T, Weinberger F (2018a) Conspecificity of the model organism Ulva mutabilis and Ulva compressa (Ulvophyceae, Chlorophyta). J Phycol 55:25–36

    Article  PubMed  Google Scholar 

  • Steinhagen S, Weinberger F, Karez R (2018b) Molecular analysis of Ulva compressa (Chlorophyta, Ulvales) reveals its morphological plasticity, distribution and potential invasiveness on German North Sea and Baltic Sea coasts. Eur J Phycol 54:102–114

    Article  Google Scholar 

  • Steinhagen S, Karez R, Weinberger F (2019) Cryptic, alien and lost species: molecular diversity of Ulva sensu lato along the German coasts of the North and Baltic Seas. Eur J Phycol 54:466–483

    Article  CAS  Google Scholar 

  • Suchard MA, Lemey P, Baele G, Ayres DL, Drummond AJ, Rambaut A (2018) Bayesian phylogenetic and phylodynamic data integration using BEAST 1.10. Virus Evol 4: vey016

  • Suzuki S, Yamaguchi H, Hiraoka M, Kawachi M (2018) Mitochondrial and chloroplast genome sequences of Ulva ohnoi, a green-tide-forming macroalga in the Southern coastal regions of Japan. Mitochondrial DNA B 3:765–767

    Article  Google Scholar 

  • Suzuki M, Segawa T, Mori H, Akiyoshi A, Ootsuki R, Kurihara A, Sakayama H, Kitayama T, Abe T, Kogame K, Kawai H, Nozaki H (2016) Next-generation sequencing of an 88-year-old specimen of the poorly known species Liagora japonica (Nemaliales, Rhodophyta) supports the recognition of Otohimella gen. nov. PLoS One 11:e0158944

  • Tonatiuh C-S, Alejandra P-G, James TM, III, Juan Manuel L-B, Margarita C-V (2019) First report, along with nomenclature adjustments, of Ulva ohnoi, U. tepida and U. torta (Ulvaceae, Ulvales, Chlorophyta) from northwestern Mexico. Bot Mar 62:113–123

  • Tran TL-A, Leliaert F, Vieira C, Tran VT, Nguyen VT, Dam DT, De Clerck O (2021) Molecular assessment of Ulva (Ulvales, Chlorophyta) diversity in Vietnam including the new species U. vietnamensis. Phycol Res (Under Review)

  • Turland N, Wiersema J, Barrie F, Greuter W, Hawksworth D, Herendeen P, Knapp S, Kusber W-H, Li D-Z, Marhold K, May T, McNeill J, Monro A, Prado J, Price M, Smith G (2018) International Code of Nomenclature for algae, fungi, and plants (Shenzhen Code) adopted by the Nineteenth International Botanical Congress Shenzhen, China, July 2017 . Regnum Vegetabile 159. Koeltz Botanical Books, Glashütten

  • Vieira C, Camacho O, Wynne MJ, Mattio L, Anderson RJ, Bolton JJ, Sansón M, D’Hondt S, Leliaert F, Fredericq S, Payri C, De Clerck O (2016) Shedding new light on old algae: Matching names and sequences in the brown algal genus Lobophora (Dictyotales, Phaeophyceae). Taxon 65:689–707

    Article  Google Scholar 

  • Wichard T, Charrier B, Mineur F, Bothwell JH, Clerck OD, Coates JC (2015) The green seaweed Ulva: a model system to study morphogenesis. Front Plant Sci 6:72

    Article  PubMed  PubMed Central  Google Scholar 

  • Xie WF, Wu CH, Zhao J, Lin XY, Jiang P (2020) New records of Ulva spp. (Ulvophyceae, Chlorophyta) in China, with special reference to an unusual morphology of U. meridionalis forming green tides. Eur J Phycol 55:412–425

    Article  Google Scholar 

  • Zhang J, Kapli P, Pavlidis P, Stamatakis A (2013) A general species delimitation method with applications to phylogenetic placements. Bioinformatics (Oxford) 29:2869–2876

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Acknowledgements

The authors gratefully acknowledge comments from Prof. Jeffery Hughey and Prof. Paul W. Gabrielson that greatly improved the manuscript.

Funding

This work was supported by the Doctoral Fellowship from Ghent University (BOF Special Research Fund) to Lan-Anh T. Tran.

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Authors and Affiliations

  1. Phycology Research Group and Center for Molecular Phylogenetics and Evolution, Ghent University, Krijgslaan 281-S8, 9000, Ghent, Belgium

    Lan-Anh T. Tran, Olivier De Clerck & Frederik Leliaert

  2. Institute of Tropical Biology, Vietnam Academy of Sciences and Technology, Hochiminh City, Vietnam

    Lan-Anh T. Tran & Tu Van Nguyen

  3. Research Institute for Basic Sciences, Jeju National University, Jeju, 63243, Korea

    Christophe Vieira

  4. Department of Marine Sciences-Tjärnö Marine Laboratory, University of Gothenburg, Strömstad, Sweden

    Sophie Steinhagen

  5. School of Biological Sciences and Queen’s, University Marine Laboratory Portaferry, Queen’s University Belfast, Northern Ireland, BT7 1NN, UK

    Christine A. Maggs

  6. Usa Marine Biological Institute, Kochi University, 194 Inoshiri, Usa, Tosa, Kochi, 781-1164, Japan

    Masanori Hiraoka

  7. Faculty of Core Research, Natural Science Division, Ochanomizu University, 2-1-1 Otsuka, Bunkyo, Tokyo, 112-8610, Japan

    Satoshi Shimada

  8. Meise Botanic Garden, Meise, Belgium

    Frederik Leliaert

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  1. Lan-Anh T. Tran
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  4. Christine A. Maggs
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  5. Masanori Hiraoka
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  9. Frederik Leliaert
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Contributions

Lan-Anh T. Tran: conceptualization, data acquisition, formal analysis, writing-original draft, review and editing. Christophe Vieira: conceptualization, formal analysis, review and editing. Frederik Leliaert and Olivier De Clerck: conceptualization, review and editing. Sophie Steinhagen, Christine A. Maggs, Masanori Hiraoka, Satoshi Shimada, and Tu Van Nguyen: review and editing.

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Correspondence to Lan-Anh T. Tran, Olivier De Clerck or Frederik Leliaert.

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Supplementary file1 Table S1: Species names mentioned in this article with authorities (XLSX 56 KB)

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Supplementary file2 Table S2: Unique haplotypes including information on the number of available sequences and names associated with the sequences. Names of GenBank sequences were restructured as follows: Genus name_species name_specimen voucher (if available)_GenBank accession number x an unique number to link specimens across three markers (if present) (XLSX 64 KB)

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Supplementary file3 Table S3: Summary of species delimitation results using GMYC and PTP methods for the tufA, rbcL and ITS markers. For each method, the numbers indicate the cluster sequences belong to (i.e. sequences having the same number belong to the same cluster). Names of GenBank sequences were restructured as follows: Genus name_species name_specimen voucher (if available)_GenBank accession number x a unique number to link specimens across three markers (if presence) (XLSX 86 KB)

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Supplementary file4 Table S4: Summary of sequences used in the comparison of species delimitation (SD) across three markers and the SD results. Colors represent conflicting results between markers: light/dark grey and light/dark blue indicate conflict between ITS and rbcL (one cluster defined by ITS but more than one defined by rbcL or vice versa) while light/dark yellow indicates conflict between rbcL and tufA (one cluster defined by rbcL but more than one defined by tufA or vice versa) (XLSX 41 KB)

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Supplementary file5 Table S5: Taxon names applied to rbcL, ITS and tufA sequences in GenBank (data downloaded on 03 December 2020), with indication of their status according to AlgaeBase (C: currently accepted, S: synonym, P: preliminary entry, U: uncertain taxonomic status, - : no information/sub-species names) (XLSX 15 KB)

Supplementary file6 Table S6: Summary of Ulva genomes available on public database (XLSX 13 KB)

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Supplementary file7 Figure S1: Name usage of Ulva species based on Google Scholar (accessed on 25 November 2020). The y axis shows species names while the x axis shows number of citations. Species of which the types have been sequenced are indicated with asterisks (PDF 30 KB)

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Supplementary file8 Figure S2: Name usage based on metadata of Ulva sequences in GenBank/ENA/DDBJ (accessed on 3 December 2020). The x axis shows number of sequences while the y axis shows species names associated with these sequences (PDF 257 KB)

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Supplementary file9 Figure S3: Genetic distance of Ulva and its sister species, namely Ochlochaete, Percursaria, Ruthnielsenia, Ulvaria, and Umbraulva, based on ITS, rbcL, and tufA markers retrieved from GenBank in August and September 2018 (PDF 73 KB)

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Tran, LA.T., Vieira, C., Steinhagen, S. et al. An appraisal of Ulva (Ulvophyceae, Chlorophyta) taxonomy. J Appl Phycol 34, 2689–2703 (2022). https://doi.org/10.1007/s10811-022-02815-x

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