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Ribosomal Dna Phylogeny of the Bangiophycidae (Rhodophyta) and the Origin of Secondary Plastids1

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Ribosomal Dna Phylogeny of the Bangiophycidae (Rhodophyta) and the Origin of Secondary Plastids1 American Journal of Botany 88(8): 1390±1400. 2001. RIBOSOMAL DNA PHYLOGENY OF THE BANGIOPHYCIDAE (RHODOPHYTA) AND THE ORIGIN OF SECONDARY PLASTIDS1 KIRSTEN M. MUÈ LLER,2,6 MARIANA C. OLIVEIRA,3 ROBERT G. SHEATH,2 AND DEBASHISH BHATTACHARYA4,5 2Department of Botany and Dean's Of®ce, University of Guelph, Guelph, Ontario, Canada, N1G 2W1; 3Department of Botany, Institute of Biosciences, University of SaÄo Paulo, R. MataÄo, Travessa 14, N. 321, SaÄo Paulo, SP, Brazil, CEP 05508-900; and 4Department of Biological Sciences, University of Iowa, 239 Biology Building, Iowa City, Iowa 52242-3110 USA We sequenced the nuclear small subunit ribosomal DNA coding region from 20 members of the Bangiophycidae and from two members of the Florideophycidae to gain insights into red algal evolution. A combined alignment of nuclear and plastid small subunit rDNA and a data set of Rubisco protein sequences were also studied to complement the understanding of bangiophyte phylogeny and to address red algal secondary symbiosis. Our results are consistent with a monophyletic origin of the Florideophycidae, which form a sister-group to the Bangiales. Bangiales monophyly is strongly supported, although Porphyra is polyphyletic within Bangia. Ban- giophycidae orders such as the Porphyridiales are distributed over three independent red algal lineages. The Compsopogonales sensu stricto, consisting of two freshwater families, Compsopogonaceae and Boldiaceae, forms a well-supported monophyletic grouping. The single taxon within the Rhodochaetales, Rhodochaete parvula, is positioned within a cluster containing members of the Erythropelti- dales. Analyses of Rubisco sequences show that the plastids of the heterokonts are most closely related to members of the Cyanidiales and are not directly related to cryptophyte and haptophyte plastid genomes. Our results support the independent origins of these secondary algal plastids from different members of the Bangiophycidae. Key words: Bangiophycidae; phylogeny; plastid; Rhodophyta; Rubisco; secondary symbiosis; small subunit rRNA. The Rhodophyta (red algae) form a distinct eukaryotic lin- characters that are considered to have been present in the an- eage (Bhattacharya et al., 1990; Van de Peer et al., 1996; Still- cestral pool of red algae and range from unicells to multicel- er and Hall, 1997) that likely shares a most recent common lular ®laments (uniseriate or multiseriate; branched or un- ancestry with the green algae (Burger et al., 1999; Moreira, branched) or sheet-like thalli (monostromatic or distromatic; Le Guyader, and Philipper, 2000). Members of the red algae Garbary, Hansen, and Scagel, 1980). Cells typically have a share a suite of characters that do not occur together in any single axial stellate plastid with a large pyrenoid, though some other eukaryote, such as a complete lack of ¯agellated stages taxa contain a cup-shaped plastid, or a complex, interconnect- and basal bodies, a two-membraned ``simple'' plastid (Bhat- ed plastid with no pyrenoid (Gantt, Scott, and Lipschultz, tacharya and Medlin, 1995) that lacks chlorophyll b or c, have 1986; Broadwater and Scott, 1994). Pit connections are rare, unstacked thylakoids with phycobilisomes, and photosynthetic and sexual reproduction has not been described in many mem- reserves stored as ¯oridean starch (Garbary and Gabrielson, bers of this subclass (Garbary, Hansen, and Scagel, 1980; Ga- 1990). Traditionally, systematists have divided the red algae brielson et al., 1990). Studies of biochemical, morphological, into two groups, sometimes with the taxonomic status of clas- and ultrastructural characters (Gabrielson and Garbary, 1985; ses, i.e., Bangiophyceae and Florideophyceae (cf. Van den Gabrielson, Garbary, and Scagel, 1985; Garbary and Gabriel- Hoek, Mann, and Jahns, 1995), or subclasses, Bangiophycidae son, 1990) and ribosomal DNA (rDNA) sequence comparisons and the Florideophycidae within a single class Rhodophyceae (Ragan et al., 1994; Oliveira et al., 1995; Oliveira and Bhat- (Gabrielson, Garbary, and Scagel, 1985), with the latter ap- tacharya, 2000) suggest that the Bangiophycidae is a diverse proach being more generally accepted. The Florideophycidae assemblage of algae that includes the Florideophycidae. For includes morphologically complex red algae in orders such as this reason, only one class of red algae, the Rhodophyceae, is the Gigartinales and the Ceramiales and is widely considered recognized by some researchers (e.g., Gabrielson et al., 1990). to be a derived, monophyletic group (Garbary and Gabrielson, Nevertheless, the name Bangiophycidae continues to be used 1990; Freshwater et al., 1994; Ragan et al., 1994; Saunders to identify the early diverging red algae from which the Flor- and Kraft, 1997). ideophycidae have evolved. The Bangiophycidae have been The Bangiophycidae (bangiophytes) retain morphological divided into four orders: Bangiales, Compsopogonales, Por- phyridiales, and Rhodochaetales (Gabrielson et al., 1990; Gar- 1 Manuscript received 14 September 2000; revision accepted 2 February 2001. bary and Gabrielson, 1990). Recently, two new orders were D. B. acknowledges a grant from the Carver Foundation and M. C. O. suggested, the Cyanidiales (Seckbach and Ott, 1994), which thanks FAPESP and CNPq for research grants. R. S. was funded by NSERC is proposed to include thermophilic genera such as Galdieria and the University of Guelph and K. M. received an Ontario Graduate Schol- and Cyanidium, and the order Erythropeltidales (Garbary, arship. The authors thank E. C. Oliveira for useful comments and suggestions. Hansen, and Scagel, 1980; Silva, Basson, and Moe, 1996). The 5 Author for correspondence (Ph: 319-335-1977; FAX: 319-335-1069; e- mail: [email protected]). latter grouping is based on the greater morphological com- 6 Current address: Department of Biology, University of Waterloo, Water- plexity in members of the Compsopogonaceae than in those loo, Ontario, Canada, N2L 3G1. of the Erythrotrichiaceae. Nonetheless, Rintoul, Vis, and 1390 August 2001] MUÈ LLER ET AL.ÐEVOLUTION OF THE BANGIOPHYCIDAE (RHODOPHYTA) 1391 TABLE 1. Algae used in the present study. Taxa GenBank Order Species Collection information accession numbera Bangiophycidae Bangiales Bangia fuscopurpurea (Dillwyn) Lyngbye SAG B59.81b GBAN-AF342745 Porphyra leucosticta Thuret in Le Jolis SAG B55.88 GBAN-AF342746 Compsopogonales Boldia erythrosiphon Herndon Black River, Ontario, Canada. Coll. T. Rintoul. GBAN-AF087109 Compsopogon coeruleus (Balbis in C. A. SAG B36.94 GBAN-AF342748 Agardh) Montagne Cyanidiales Galdieria sulphuraria (Galdieri) Merola SAG 107.79 GBAN-AF342747 Porphyridiales Bangiopsis subsimplex (Montagne) Schmitz PR21, Guajataca Beach, Puerto Rico. Coll. T. GBAN-AF168627 Rintoul & A. Sherwood. 19.X.97. Chroodactylon ornatum (C. Ag.) Basson UTEX LB 1633c (5 Asterocytis ramosa) GBAN-AF168628 Chroodactylon ramosum (Thwaites) Hansgirg SAG B103.79 GBAN-AF342751 Flintiella sanguinaria F. D. Ott UTEX LB 2060 GBAN-AF168621 F. sanguinaria SAG B40.94 GBAN-AF342749 Goniotrichopsis sublittoralis Smith in Smith et UTEX LB 1689 GBAN-AF168629 Hollenberg Porphyridium aerugineum Geitler CCAP 1380/4d GBAN-AF168623 Porphyridium sordidium Geitler CCAP 1380/6 GBAN-AF168630 Rhodella violacea (Kornmann) Wehrmeyer UTEX LB 2427 GBAN-AF168624 Rhodosorus marinus Geitler CCMP 769e GBAN-AF168625 R. marinus SAG 116.79 GBAN-AF342750 Rhodosorus sp. CCMP 1530 GBAN-AF168626 Stylonema alsidiif (Zanardini) K. Drew UTEX LB 1424 GBAN-AF168633 S. alsidii (CR) Coll. R. Sheath & K. MuÈller. 17.II.98. GBAN-AF168632 Stylonema cornu-cervi Reinsch CCAP 1367/1 GBAN-AF168622 Florideophycidae Batrachospermales Nemalionopsis tortuosa Yagi et Yoneda SAG B42.94 GBAN-AF342743 Thorea violacea Bory de St. Vincent SAG 51.94 GBAN-AF342744 a The pre®x GBAN- has been added to link the online version of American Journal of Botany to GenBank but it is not part of the actual accession number. b SchloÈsser (1994). c Starr and Zeikus (1993). d http://www.ife.ac.uk/ccap. e Anderson, Morton, and Sexton (1997). f Synonyms: Stylonema 5 Goniotrichum (Wynne, 1985). Sheath (1999) provided molecular evidence that does not sup- the speci®c donor of this plastid remains unknown (see also port recognition of the Eryhtropeltidales. Oliveira and Bhattacharya, 2000). We ask, therefore, if there Previous molecular studies indicate that, whereas the Ban- is a speci®c evolutionary relationship between the nucleo- giales and Compsopogonales appear to be monophyletic, other morphs in cryptophyte algae and any of the Bangiophycidae orders, such as the Porphyridiales, may be either biphyletic or orders. The goals of this research are to present a phylogenetic paraphyletic within the Bangiophycidae (Ragan et al., 1994; hypothesis for the Bangiophycidae that can be tested in future Rintoul, Vis, and Sheath, 1999; Oliveira and Bhattacharya, studies to ultimately create a natural classi®cation of the Rho- 2000). In their analysis of red algal orders using a variety of dophyta and to gain further insights into the origin of plastids morphological, ultrastructural, and biochemical data, Gabriel- through red algal secondary symbiosis. son and Garbary (1985), Gabrielson, Garbary, and Scagel (1985), and Garbary and Gabrielson (1990) also hypothesized MATERIALS AND METHODS that the Porphyridiales were probably paraphyletic and found considerable differences in plastid ultrastructure and highly Bangiophycidae were either collected in the ®eld or obtained from the cul- variable vegetative and reproductive morphologies. They
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