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Ulvella Tongshanensis (Ulvellaceae, Chlorophyta), a New Freshwater Species from China, and an Emended Morphological Circumscription of the Genus Ulvella

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Ulvella Tongshanensis (Ulvellaceae, Chlorophyta), a New Freshwater Species from China, and an Emended Morphological Circumscription of the Genus Ulvella Fottea, Olomouc, 15(1): 95–104, 2015 95 Ulvella tongshanensis (Ulvellaceae, Chlorophyta), a new freshwater species from China, and an emended morphological circumscription of the genus Ulvella Huan ZHU1, 2, Frederik LELIAERT3, Zhi–Juan ZHAO1, 2, Shuang XIA4, Zheng–Yu HU5, Guo–Xiang LIU1* 1 Key Laboratory of Algal Biology, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan 430072, P. R. China; *Corresponding author e–mail: [email protected] 2University of Chinese Academy of Sciences, Beijing 100049, P. R. China 3Marine Biology Research Group, Department of Biology, Ghent University, Krijgslaan 281–S8, 9000 Ghent, Belgium 4College of Life Sciences, South–central University for Nationalities, Wuhan, 430074, P. R. China 5State key Laboratory of Freshwater Ecology and Biotechnology, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan 430072, P. R. China Abstract: A new freshwater species of Ulvella, U. tongshanensis H. ZHU et G. LIU, is described from material collected from rocks under small waterfalls in Hubei Province, China. This unusual species differs from other species in the genus by the macroscopic and upright parenchymatous thalli, and by the particular habitat (most Ulvella species occur in marine environments). Phylogenetic analyses of plastid encoded rbcL and tufA, and nuclear 18S rDNA sequences, pointed towards the generic placement of U. tongshanensis and also showed a close relationship with two other freshwater species, Ulvella bullata (Jao) H. ZHU et G. LIU, comb. nov. and Ulvella prasina (Jao) H. ZHU et G. LIU, comb. nov. The latter two were previously placed in the genus Jaoa and are characterized by disc–shaped to vesicular morphology. Our study once again shows that traditionally used morphological characters are poor indicators for phylogenetic relatedness in morphologically simple algae like the Ulvellaceae. Thus, the morphological circumscription of the genus Ulvella is here expanded to include: (1) thalli that are uniseriate in basal and apical parts, and parenchymatous in the middle portion with distinct differentiation of an unbranched dorsal side and a ventral side developing many short branches, and (2) epibiotic or epilithic, disc–shaped to vesicular thalli with a di– or tristromatic structure. Key words: Jaoa, Morphology, New species, Phylogeny, Ulvales, Ulvellaceae, Ulvophyceae INTRODUCTION Ochlochaete, Entocladia, Pringsheimiella to Ulvella, and emended and erected a large genus Ulvella . As The green algal family Ulvellaceae is characterized currently circumscribed, Ulvella is characterized by by prostrate, free–branching filaments, or radiating, irregularly branched, uniseriate filaments, that form compact and coherent filaments forming mono– or open branched tufts, or mono– or polystromatic disc– polystromatic discs or rosettes. Most species are shaped thalli (RINKEL et al. 2012; NIELSEN et al. 2013). found in marine or brackish habitats, growing epi– The freshwater genus Jaoa K.C.FAN (1964), which was or endophytic, epilithic on various substrates, or formally placed in a separate family, Jaoaceae Fan, has endolithic in calcareous substrates (CORREA et al. 1987, also been shown to belong to the Ulvellaceae based on 1988; NIELSEN et al. 2013). A few species are known phylogenetic analysis of 18S rDNA and rbcL sequences from freshwater habitats (ZHU et al. 2013; Mareš et al. (ZHU et al. 2013; Mareš et al. 2014). The only two 2014). species described are characterized by disc–shaped or The family was resurrected and emended hollow, vesicular thalli, up to 6 cm in diameter (JAO by O’KELLY & FLOYD (1983) to include six genera: 1941, 1947; ZHU et al. 2013). The two species in the Acrochaete, Endophyton, Endocladia, Ochlochaete, genus are morphologically distinguished by either Pringsheimiella, and Ulvella. Based on phylogenetic having a distromatic (J. prasina) or tristromatic (J. analysis of tufA sequences and morphological bullata) thallus (ZHU et al. 2013). observations of cultured plants, NIELSEN et al. (2013) In this paper, we report on a new green algal transferred most species of Acrochaete, Endophyton, species, collected on rocks under a small waterfall in 96 ZHU et al.: New species of the genus Ulvella Fottea, Olomouc, 15(1): 95–104, 2015 97 Mt. Jiugong near Tongshan Couty, Hubei province. The they are the same individual. Sequences selected based on sporangia and gametangia, were not observed. (NIELSEN et al. 2013, 2014). Phylogenetic analyses of new species is placed in the genus Ulvella, mainly based a BLAST search, along with putative relatives and a broader the tree markers recovered a highly supported Ulvella on results from our molecular phylogenetic analysis of selection of green algae were downloaded from GenBank Culture observations: Clear morphological differences (= Ulvellaceae) clade (sensu NIELSEN et al. 2013), and three markers (plastid encoded rbcL and tufA, and the (http://www.ncbi.nlm.nih.gov/). The sequences (56 18S of vegetative thalli were observed between thalli from unambiguously placed our new species within that rDNA, 14 rbcL, and 49 tufA sequences) were initially nuclear 18S rDNA). We also propose to transfer the natural habitats and plants grown under laboratory clade. Although phylogenetic relationships within aligned by ClustalX (v. 1.83) (THOMPSON et al. 1997), and only two species of the genus Jaoa (J. prasina and J. the Ulvella clade are generally weakly supported, the refined manually using Seaview (v. 4.32) G( OUY et al. 2010). culture conditions. Plants in culture grew slowly after bullata) to Ulvella. Our results call for an expansion of Mutational saturation was evaluated in the variable positions inoculation. Two types of cultural morphology were phylogenies of the three markers indicated a close the natural morphological circumscription of the genus of the three alignments by plotting pairwise distances against observed. The first type was characterized by short relationship between Ulvella tongshanensis, Ulvella Ulvella, and in extension of the family Ulvellaceae. model–corrected distances using TAMURA and NEI (1993) and filaments consisting of a vegetative cells with a similar (Jaoa) prasina and Ulvella (Jaoa) bullata. KIMURA (1980) models estimated in MEGA (v.5.0) (TAMURA morphology as thalli from natural habitat: robust cells The phylogenetic placement of the two Jaoa species et al. 2011). The result showed that neither transitions nor with length/width ratio 0.4–1.5. Branches at this stage (including the type, J. prasina) warrants the transfer transversions have reached saturation. Phylogenies were were short and consisted of 2–5 cells (Figs 15–16). to Ulvella. MATERIALS AND METHODS estimated using maximum likelihood (ML) in PAUP4.0* The second type was characterized by long lateral (v.4.0 beta) (SWOFFORD 1998) and Bayesian inference (BI) branches consisting of slender cells, 5–11 µm wide Ulvella prasina (JAO) H. ZHU et G. LIU comb. nov. Algal samples were collected in Jiugong Moutain Nature in MrBayes (v. 3.1.2) (HUELSENBECK et al. 2001). Modeltest and 26–72 µm long, growing prostrate and irregularly Basionym: Coelodiscus prasinus JAO, Studies on the fresh–water Conservation area (29º40'N, 114º25'E), Tongshan County, (v.3.06) (POSADA & CRANDAL 1998) was executed to select the algae of China IX. Coelodiscaceae. Sinensia, 12: 291–298, 1941. Hubei Province on rocks under a small waterfall in June, 2013. best–fit evolutionary model under the Hiearchial Likelihood on solid culture medium (Figs 17–18). The centeral Synonym: Jaoa prasina (JAO) FAN, Acta Phytotax. Sinica, 9 (1): 101, Samples were kept cool and transferred to the laboratory on Ratio Tests (hLRTs) and Akaike Information Criterion (AIC). part of the thalli consisted of many globular cells (Fig. 1964. the same day. Samples were rinsed in PBS buffer (pH = 7.0) The best–fit models were GTR+I+G for 18S rDNA andrbc L, 17, arrowhead). Initiation of reproduction failed on several times to remove epiphytes and sediment. Then, the and GTR+I for tufA. For ML analysis, a heuristic search BBM or BG–11 medium. Acrochaete–type hairs were Ulvella bullata (JAO) H. ZHU et G. LIU, comb. nov. alga was inoculated on BG–11 medium (ALLEN 1968) with option with random addition of sequences (10 replicates) observed in thalli grown in nitrogen–deficient medium Basionym: Coelodiscus bullatus JAO, Bot. Bull. Acad. Sinica, 1: 1.5% agar in plastic Petri dishes under a constant light source and the tree bisection and reconnection branch–swapping (Figs 19–20, arrowheads), but not in thalli grown in 255–256, f.1, 1947. of 50 μmol.m–2.s–1 and a temperature of 20 °C. To obtain algorithm were used for tree searching. Bootstrap analysis regular BBM and BG–11 medium. Synonym: Jaoa bullata (JAO) FAN, Acta Phytotax. Sinica, 9 (1): 101, unialgal culture, clean filaments were cut and transferred to with 1000 replicates of the dataset for ML was performed 1964. new medium several times. The culture strain was deposited to estimate statistical reliability. A Bayesian Markov Chain in the Freshwater Algae Culture Collection, Institute of Monte Carlo analysis was run with four Markov chains (three Etymology: The species epithet refers to the Holotype Hydrobiology, Chinese Academy of Sciences (FACHB) heated chain, one cold) for 20 million generations with tree locality (Tongshan County). under accession No. FACHB–1780. sampling every 10000 generations. The stationary distribution Type locality: Jiugong Moutain Nature Conservation DISCUSSION To observe the asexual and sexual reproduction, the was assumed when the
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