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Rindi Et Al. 2004.Pdf J. Phycol. 40, 977–997 (2004) r 2004 Phycological Society of America DOI: 10.1111/j.1529-8817.2004.04012.x THE PRASIOLALES (CHLOROPHYTA) OF ATLANTIC EUROPE: AN ASSESSMENT BASED ON MORPHOLOGICAL, MOLECULAR, AND ECOLOGICAL DATA, INCLUDING THE CHARACTERIZATION OF ROSENVINGIELLA RADICANS (KU¨ TZING) COMB. NOV.1 Fabio Rindi, Lynne McIvor2, and Michael D. Guiry3 Department of Botany, Martin Ryan Institute, National University of Ireland, Galway, Ireland Despite a simple morphology and intensive stud- The Prasiolales is an order of marine, freshwater, ies carried out for more than two centuries, the sys- and terrestrial green algae widespread in polar and tematics of the Prasiolales still presents several cold temperate regions (Burrows 1991, Sherwood unsolved problems. The taxonomic relationships et al. 2000), characterized by a stellate axial chlorop- of several common species of Prasiolales, mostly last with a central pyrenoid, flagellate cells with four from northern Europe, were investigated by a com- microtubular roots in a cruciate arrangement and an- bination of morphological observations, culture ex- ticlockwise rotation of basal bodies, closed mitosis with periments, and molecular analyses based on rbcL a persistent telophase spindle, and cytokinesis by trans- sequences. The results indicate that Rosenvingiella verse wall deposition (O’Kelly et al. 1989, van den and Prasiola are separate genera. The capacity for Hoek et al. 1995, Sherwood et al. 2000). Its phyloge- production of tridimensional pluriseriate game- netic affinities are not yet completely clear, but recent tangia and the presence of unicellular rhizoids are molecular evidence indicates that the Trebouxiophy- the morphological features that discriminate Rose- ceae is the class to which the Prasiolales is most closely nvingiella from filamentous forms of Prasiola. The related (Sherwood et al. 2000, Friedl and O’Kelly molecular data indicate that uniseriate filaments 2002). can be produced in at least three different species Although relatively simple, the morphology of the of Prasiola. The genetic diversity of uniseriate fila- Prasiolales is very diverse and includes uniseriate fila- mentous Prasiolales is higher than their simple ments, narrow ribbons, expanded blades, and sarcinoid morphology would indicate, and the provisional re- colonies (van den Hoek et al. 1995). As presently cir- tention of Schizogonium Ku¨tzing 1843 as independ- cumscribed, the order contains four widely accepted ent genus is recommended. The rbcL phylogeny genera: Prasiococcus Vischer, Prasiola Meneghini, Prasiolo- confirms that Prasiola calophylla, P. crispa,and psis Vischer, and Rosenvingiella P. C. Silva. The validity of P. stipitata are distinct species, whereas P. stipitata a fifth genus, Schizogonium Ku¨tzing, is disputed, and and P. meridionalis are probably conspecific. Rose- despite recommendations to retain it as an independ- nvingiella polyrhiza is a strictly marine alga, and ent genus (Silva 1980), in more recent literature it most records of Rosenvingiella in Europe are refer- is usually not considered, having been apparently able to Rosenvingiella radicans, proposed here as a regarded as a developmental stage of Prasiola and new combination based on Ulothrix radicans Ku¨tz- Rosenvingiella (Burrows 1991). ing 1849. This is a primarily terrestrial alga that can The circumscription of prasiolalean taxa at both occur from upper intertidal rock to locations situ- species and genus levels remains one of the most prob- ated hundreds of kilometers inland. The great con- lematic areas in green algal taxonomy, as these algae fusion that has arisen in Europe between these two show considerable morphological plasticity (Burrows species in the last century is mostly due to misiden- 1991, Hamilton and Edlund 1994, Kova´ˇcik and Batista tifications of marine populations of R. radicans. Pereira 2001). Over the last 150 years, the taxonomic Key index words: Chlorophyta; distribution; Eu- relationships of filamentous and blade-like forms of rope; phylogeny; Prasiola; Prasiolales; rbcL gene; Prasiolales have been examined in detail, and several Rosenvingiella; Schizogonium; subaerial algae monographic studies on this group have been pub- lished (Jessen 1848, Imha¨user 1889, Knebel 1935). Abbreviations: BP, bootstrap proportions; ML, Despite this, many problems, at both the genus and maximum likelihood; MP, maximum parsimony; species levels, still remain to be resolved. NJ, neighbor joining; rbcL, gene of the large subunit The genus Prasiola was established by Meneghini of RUBISCO (1938, p. 36) for a group of leafy green algae formerly considered a tribe of Ulva (Agardh 1823, p. 416). Al- though the original concept of the genus was limited to blade-like forms, it was realized that the leafy mor- 1Received 30 January 2004. Accepted 2 July 2004. 2Present address: Nationaal Herbarium Nederland, Universiteit phology may show a transition to different morpho- Leiden branch, Einsteinweg 2, 2300 RA, Leiden, The Netherlands. types as early as in the first half of the 19th century 3Author for correspondence: e-mail [email protected]. (Agardh 1828, p. 44, Ku¨tzing 1843, p. 246). Prasiola 977 978 FABIO RINDI ET AL. crispa in particular, the lectotype species of Prasiola (Si- 2004b). Because this species shows the characteristic lva 1980), occurs as both uniseriate filaments and ex- features of Rosenvingiella (transversal division of the panded blades, with a complete range of intermediate axial cells and production of pseudo-parenchymatous forms (West 1916, Knebel 1935, Kobayasi 1967, Bur- gametangia), we concluded that it was a terrestrial rows 1991). form of Rosenvingiella polyrhiza (Rindi et al. 1999, Rindi Rosenvinge (1893) erected the genus Gayella for fil- and Guiry 2003). It was recognized, however, that this amentous prasiolalean algae able to produce pseudo- conclusion was not completely satisfactory, because its parenchymatous gametangia by transversal divisions of morphology is not in perfect agreement with the fea- uniseriate filaments. Because Gayella Rosenvinge is a tures of the material originally described by Rose- later homonym of Gayella Pierre (Sapotaceae, Ma- nvinge (1893) from Greenland. gnoliophyta), the genus was subsequently renamed Taxonomic problems also exist in Prasiola sensu Rosenvingiella by Silva (1957). Whether Rosenvingiella stricto. The relationships at species level between constitutes a separate genus from Prasiola remains con- some European species of Prasiola are not yet com- troversial. In Europe, the notion that Rosenvingiella po- pletely clear. It has been suggested by some authors lyrhiza (Rosenvinge) P. C. Silva, the generitype, may that Prasiola calophylla (Carmichael ex Greville) Ku¨tzing represent a developmental stage of Prasiola has arisen and P. stipitata Suhr ex Jessen might be conspecific because it occurs frequently mixed with species of (Waern 1952, Edwards 1975), with P. stipitata being Prasiola and intermediates seem to occur between considered as a marine form of P.calophylla. It has also them (Brgesen 1902, Edwards 1975, Burrows 1991, been proposed that P.stipitata may possibly be conspe- John 2002). Wille (1901), apparently in ignorance of cific with some extra-European species, such as P. Rosenvinge’s work, described Prasiola crispa f. submarina meridionalis (Bravo 1965). for an alga clearly corresponding to Rosenvingiella. It is therefore evident that despite two centuries of Brgesen (1902) created the new name Prasiola crispa intensive work, many problems concerning the taxon- subsp. marina for the same alga and placed Gayella po- omy of European Prasiolales remain to be resolved. lyrhiza in synonymy. He was followed in this by Cotton The application of molecular techniques to algal sys- (1912) and Newton (1931). More recently, Edwards tematics has now proven fundamental for investigating (1975) supported the hypothesis of a relationship be- algal phylogenetics and has shed light on many tax- tween Rosenvingiella and Prasiola, although not specify- onomic problems in different algal groups. The DNA ing it in detail, and Ettl and Ga¨rtner (1995) also listed sequences of the plastid encoded RUBISCO (rbcL) Gayella polyrhiza as a synonym of Prasiola crispa.Other gene, in particular, have proven useful for elucidation authors, however (Collins 1909, Setchell and Gardner of relationships at the species and genus level and have 1920a, Knebel 1935, Waern 1952, Kornmann and Sah- been successfully used for several groups of green al- ling 1974, Womersley 1984, Burrows 1991), regarded gae (McCourt et al. 2000, Hayden and Waaland 2002, Rosenvingiella and Prasiola as separate genera, and all Hoham et al. 2002, Sernepont Domis et al. 2003, recent lists of northern European seaweeds include Zechman 2003, Sakayama et al. 2004). In the present Rosenvingiella polyrhiza as a species independent of P. study, we combine the use of rbcL sequences with mor- crispa (Nielsen et al. 1995, Bartsch and Kuhlenkamp phological and ecological data for the investigation of 2000, Gunnarsson and Jonsson 2002, Hardy and Guiry the relationships between genera and species currently 2003, Rindi and Guiry 2004a). Similar problems are placed in the Prasiolales. The results presented here found on the Pacific coast of North America with re- provide a definitive answer to several problems that gard to the relationship between Rosenvingiella constricta have plagued green algal taxonomists for more than (Setchell & Gardner) P.C. Silva and Prasiola meridionalis two centuries. Setchell
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