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Tortula and Some Related Genera (Pottiaceae, Musci): Phylogenetic Relationships Based on Chloroplast Rps4 Sequences

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Tortula and Some Related Genera (Pottiaceae, Musci): Phylogenetic Relationships Based on Chloroplast Rps4 Sequences Plant Syst. Evol. 235: 197–207 (2002) DOI 10.1007/s00606-002-0230-0 Tortula and some related genera (Pottiaceae, Musci): phylogenetic relationships based on chloroplast rps4 sequences O. Werner, R. M. Ros, M. J. Cano, and J. Guerra Departamento de Biologı´ a Vegetal (Bota´ nica), Facultad de Biologı´ a, Universidad de Murcia, Spain Received May 23, 2002; accepted August 23, 2002 Published online: November 22, 2002 Ó Springer-Verlag 2002 Abstract. According to chloroplast rps4 sequence by a peristome of 16 mainly erect cleft teeth, data the genus Syntrichia forms a monophyletic stretching from near the base or from a low clade clearly separated from Tortula, while Pottia is basal membrane up to the apex, becoming shown to be polyphyletic and the Rhynchostegiae divided into two filaments. Pottia (Rchb.) species (with rostrate lid) are very similar to Ehrh. ex Fu¨ rn. has been separated by the Tortula. Crossidium is probably polyphyletic. The presence of a cleistocarpous or stegocarpous close affinity of Desmatodon, Stegonia, Pterygoneu- capsule (gymnostomous or with a peristome of rum and some of the species of Phascum with Tortula is confirmed by the molecular data. 16 imperfect or lanceolate bifid teeth) and Tortula Hedw. has been characterised by 32 Key words: Bryophyta, Pottiaceae, Tortula, Cros- filiform twisted teeth, united at the base into a sidium, Pottia, molecular phylogeny, rps4. tubular membrane of varying length. Also, some authors have considered the genus Syn- trichia Brid. for including the species of Tortula with a twisted peristome from a high spirally Introduction tessellated tube (Agnew and Vondra´ cˇ ek 1975). The generic boundaries in the Tribe Pottieae However, this separation has not been satis- (Limpr.) Dixon of the subfamily Pottioideae factory and there is controversy on the taxa (Limpr.) Broth., family Pottiaceae Bruch & that should be included in each genus. Schimp., notably in the series Pottia-Desmato- In his new treatment of the Pottiaceae don-Tortula-Syntrichia are particularly difficult genera, in which the gametophytic characters to delimit (Blockeel 1990), as the taxonomy of were emphasized, Zander (1989, 1993) con- these genera is mainly based on their sporo- vincingly proposed some characters to segre- phytic characters, more specifically on the gate genera such as Chenia R. H. Zander and height of the basal membrane of the peristome Syntrichia from Tortula. According to this and on the patterns which the teeth follow author, Chenia differs from Tortula in its when they divide above this membrane dentate upper leaf margins, large epapillose (Limpricht 1890, Mo¨ nkemeyer 1927, Lawton laminal cells, thin costa, and red KOH 1971, Smith 1978, Nyholm 1989). Thus, the reaction of the upper laminal cells, while genus Desmatodon Brid. has been characterised Syntrichia differs in the crescent shape of the 198 O. Werner et al.: Phylogenetic relationships of Tortula and related genera stereid band in the leaf transverse section, Material and methods lack of differentiated dorsal epidermal cells, Plant material. 36 sequences representing 35 taxa and red KOH reaction. On the other hand, were included in this study. A previous study this author included in Tortula sect. Pottia based on rps4 sequences representing a great (Rchb.) Kindb. taxa that had traditionally range of the Pottiaceae (unpublished data) sug- been placed in other genera, such as Pottia gests that the clade studied here is monophyletic. (the species with rostrate lid, named by Barbula unguiculata Hedw. was chosen as out- Warnstorf (1916) as Rhynchostegiae)or group species because it was situated in the sister Phascum Hedw. (Phascum cuspidatum clade. Hedw.), but with gametophytic characters Table 1 lists all taxa used in this study, the very similar to those of Tortula. For the voucher specimen data or reference, the origin same reason, he included the genus Desmato- and GenBank accession numbers. Vouchers are don in Tortula sect. Tortula Broth. deposited at MUB. DNA isolation. Total DNA was extracted There is general agreement concerning from dry material using the DNeasy Plant Mini some taxonomic changes and phylogenetic Kit of Qiagen (Hilden, Germany). The DNA was considerations provided by Zander (1993) eluted in 100 ll of 10 mM Tris-buffer (pH 8.5) and (e.g. the separation of Syntrichia from Tortula) stored in the freezer until amplification. although other aspects such as the relation of Amplification. The chloroplast rps4 gene was Pottia, Phascum and Desmatodon with Tortula amplified in a 50 ll final volume with the primers are more debatable. Also, the relationships rps5 (Nadot et al. 1994) and trnas (Buck et al. between some genera of Pottieae, whose origin 2000). 1 ll of stock DNA was added as template. has been supposed to be close to a Tortula-like The amplification conditions were as follows: ancestor (Delgadillo 1975, Frey et al. 1990, 3min at 94 °C, 35 cycles with 15 sec 94 °C, Cano et al. 1993, Zander 1993) remain unre- 30 sec 50 °C and 1 min 72 °C, and a final 7- solved. This is the case with the genera min extension step at 72 °C. Amplification pro- ducts were controlled on 8% PAA gels, and Crossidium Jur. and Pterygoneurum Jur., successful reactions were cleaned with the help of which differ from Tortula in the presence of the High Pure PCR Product Purification Kit supranervial filaments or lamellae, respective- of Roche Molecular Biochemicals (Mannheim, ly. Aloina Kindb. also presents this kind of Germany). chlorophyllic structures on the ventral side of Sequencing and data analysis. Cycle sequenc- the lamina but is excluded from our study ing was performed with the Big Dyes Sequencing because previous DNA assays made by the Kit (Perkin Elmer) using a standard protocol and authors (Werner et al. unpublished) demon- the amplification primers. The aligning tempera- strated that this genus does not belong to the tures were set to 60 °C in the case of rps5 and 55 °C group of genera closely related to Tortula.In in the case of trnas. The reaction products were addition, Stegonia Venturi has been supposed separated on a ABI Prism 3700 automatic to be related to Pottia by some authors sequencer (Perkin Elmer). The sequences were edited using Bioedit 5.0.9 (Hall 1999) and aligned (Limpricht 1890, Mo¨ nkemeyer 1927, Chen manually. The data are available from the corre- 1941, Wareham 1972). However, it has been sponding author on request. The aligned sequences treated as an independent genus by other were analysed using Neighbor-Joining (NJ; Saitou recent authors, such as Smith (1978), Nyholm and Nei 1987), Maximum Parsimony (MP; Fitch (1989) and Zander (1993). 1971) and Bayesian inference (Bayes 1763). In the The purpose of the present paper is to case of NJ we used PAUP* (Swofford 1998), with provide a new and independent dataset (chlo- distance ¼ hky85, objective ¼ LSFIT, power ¼ 2. roplast rps4 sequence) to clarify the circum- A bootstrap analysis with 1000 replicates was run. scription of the genus Tortula and the The MP analysis, run with PAUP*, used the phylogenetic relationships between Tortula following settings: RANDOM additions, TBR and some related genera. branch-swapping, MULTREES ¼ yes, steepest Table 1. Taxa included in the rps4 sequence analysis. All sequences are submitted to GenBank O. Werner et al.: Phylogenetic relationships of Species Voucher Origin GenBank # or reference Barbula unguiculata Hedw. MUB 10325 Germany, Baden-Wu¨ rttemberg AF480952 Crossidium aberrans Holz. & E.B. Bartram MUB 6089 Spain, Albacete AF481006 Crossidium crassinerve (De Not.) Jur. MUB 11622 Morocco, Anti-Atlas AF481045 Crossidium davidai Catches. MUB 5349 Spain, Canary Islands, Lanzarote AF481005 Crossidium laevipilum The´ r. & Trab. MUB 11665 Morocco, Anti-Atlas AF481046 Crossidium seriatum H.A. Crum & Steere UNLV, Arizona U.S.A., Arizona AF481007 Crossidium seriatum H.A. Crum & Steere MUB 4354 Spain, Albacete AF481010 Crossidium squamiferum (Viv.) Jur. MUB 7982 Spain, Huelva AF481004 Desmatodon latifolius (Hedw.) Brid. MUB 11476 Spain, Granada AF480954 Leptophascum leptophyllum (Mu¨ ll. Hal.) MUB 10427 Spain, Murcia AF480960 J. Guerra & M.J. Cano Microbryum curvicolle (Hedw.) R.H. Zander MUB 8269 Spain, Almerı´ a AF480971 Microbryum davallianum (Sm.) R.H. Zander MUB 12537 Spain, Alicante AF480983 Microbryum rectum (With.) R.H. Zander MUB 11199 Spain, Valencia AF480970 Tortula Phascum cuspidatum Hedw. MUB 11344 Spain, Sevilla AF480972 Pottia intermedia (Turner) Fu¨ rnr. MUB 5430 Germany, Nordrhein Westfalen AF481013 and related genera 199 Pottia lanceolata (Hedw.) Mu¨ ll. Hal. MUB 10334 Spain, Murcia AF480988 Pottia pallida Lindb. MUB 8768 Spain, Almerı´ a AF480987 Pottia truncata (Hedw.) Bruch & Schimp. MUB 10336 Spain, Cadiz AF481044 Pottia wilsonii (Hook.) Bruch & Schimp. MUB 8740 Spain, Almerı´ a AF481011 Protobryum bryoides (Dicks.) MUB 4936 Spain, Alicante AF480986 J. Guerra & M.J. Cano Pterygoneurum lamellatum (Lindb.) Jur. MUB 11484 Spain, Murcia AF480959 Stegonia latifolia (Schwa¨ gr.) Venturi ex Broth. La Farge et al. (2000) - AF222901 Syntrichia ammonsiana (H.A. Crum MUB 12225 South Africa, AF480957 & L.E. Anderson) Ochyra Western Cape Prov. Syntrichia caninervis Mitt. MUB 10977 Spain, Guadalajara AF480958 Syntrichia leucostega (Mu¨ ll. Hal.) R.H. Zander MUB 12226 South Africa, AF480982 Western Cape Prov. Syntrichia montana Nees MUB 10881 Morocco, Rif AF481031 Syntrichia papillosa (Wils.) Jur. MUB 12227 South Africa, AF481032 Western Cape Prov. Syntrichia rigescens (Broth. & Geh.) Ochyra MUB 11378 Morocco, High-Atlas AF481037 Syntrichia
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