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Downloaded from Genbank ( Org Divers Evol (2016) 16:481–495 DOI 10.1007/s13127-015-0258-y ORIGINAL ARTICLE A phylogeny of Lophocoleaceae-Plagiochilaceae-Brevianthaceae and a revised classification of Plagiochilaceae Simon D. F. Patzak1 & Matt A. M. Renner2 & Alfons Schäfer-Verwimp3 & Kathrin Feldberg1 & Margaret M. Heslewood2 & Denilson F. Peralta4 & Aline Matos de Souza5 & Harald Schneider6,7 & Jochen Heinrichs1 Received: 3 October 2015 /Accepted: 14 December 2015 /Published online: 11 January 2016 # Gesellschaft für Biologische Systematik 2016 Abstract The Lophocoleaceae-Plagiochilaceae- radiculosa; this species is placed in a new genus Brevianthaceae clade is a largely terrestrial, Cryptoplagiochila. Chiastocaulon and a polyphyletic subcosmopolitan lineage of jungermannialean leafy liver- Acrochila nest in Plagiochilion; these three genera are worts that may include significantly more than 1000 spe- united under Chiastocaulon to include the Plagiochilaceae cies. Here we present the most comprehensively sampled species with dominating or exclusively ventral branching. phylogeny available to date based on the nuclear ribosom- The generic classification of the Lophocoleaceae is still al internal transcribed spacer region and the chloroplast unresolved. We discuss alternative approaches to obtain markers rbcLandrps4 of 372 accessions. Brevianthaceae strictly monophyletic genera by visualizing their consis- (consisting of Brevianthus and Tetracymbaliella)forma tence with the obtained consensus topology. The present- sister relationship with Lophocoleaceae; this lineage is in ed phylogeny will serve as a basis for follow-up studies turn sister to Plagiochilaceae. Plagiochila is resolved including several thousand accessions. These studies will monophyletic subsequent to exclusion of Plagiochila enable revision of current hypotheses on species diversity and distribution of Lophocoleaceae-Plagiochilaceae- Brevianthaceae and allow for a reconstruction of their Electronic supplementary material The online version of this article (doi:10.1007/s13127-015-0258-y) contains supplementary material, evolution in time and space. which is available to authorized users. Keywords Acrochila . Bryophyte . Chiastocaulon . * Jochen Heinrichs Chiloscyphus . Cryptoplagiochila . Genus concept . [email protected] Liverwort . Plagiochilion 1 Faculty of Biology, Department of Biology and Geobio-Center, Ludwig Maximilian University, Menzinger Str. 67, In recent years, molecular phylogenies have revolutionized 80638 Munich, Germany our understanding of liverwort evolution and relation- 2 Royal Botanic Gardens and Domain Trust, Mrs Macquaries Road, ships (Davis 2004; Heinrichs et al. 2005a; Hentschel et al. Sydney, NSW 2000, Australia 2006a; He-Nygrén et al. 2006; Feldberg et al. 2010b; 3 Mittlere Letten 11, 88634 Herdwangen-Schönach, Germany Vanderpoorten et al. 2010; Devos et al. 2011;Cooperetal. 4 Instituto de Botânica, Caixa Postal 68041, 04045-972 São Paulo, SP, 2012;Dongetal.2013;Shawetal.2015). Studies at all Brazil taxonomic levels have identified incongruence between 5 Departamento de Ciências Biológicas, Avenida Transnordestina s/n, morphology-based classifications and molecular-based phylo- Novo Horizonte, Universidade Estadual de Feira de Santana, genetic hypotheses, with the result that comprehensive 44036-900 Feira de Santana, BA, Brazil amendments have been made to morphology-based classifica- 6 Department of Life Science, Natural History Museum, tion systems from species (Heinrichs et al. 2004b; Preussing London SW75BD, UK et al. 2010; Ramaiya et al. 2010;Renneretal.2011, 2013a) 7 School of Life Sciences, Sun Yatsen University, through subgenera (Devos et al. 2011; Heinrichs et al. 2012), Guangzhou 510275, Guandong, China genera (Hentschel et al. 2007;Feldbergetal.2010b; Preussing 482 S.D.F. Patzak et al. et al. 2010), family (Hentschel et al. 2006a; Hendry et al. R.M. Schust. based on its androecia and gynoecia restricted 2007), order and class (Heinrichs et al. 2005a; He-Nygrén to highly abbreviated lateral-intercalary branches lacking veg- et al. 2006; Crandall-Stotler et al. 2009). The rapid accumula- etative leaves, strictly lateral-intercalary branching, scattered tion of molecular data presents opportunities to further im- rhizoids and a supposed complete lack of underleaves (Engel prove current classification systems by testing the monophyly and Schuster 1982). Molecular phylogenies found of and relationships between established and recently pro- Brevianthus J.J. Engel & R.M. Schust. sister to the posed taxonomic entities on the basis of an effectively inde- Lophocoleaceae element Tetracymbaliella Grolle (He- pendent data source. Nygrén et al. 2006). Based on this topology, Söderström Molecular phylogenetic studies identified a monophyletic et al. (2013) transferred Tetracymbaliella to Brevianthaceae. lineage of jungermannialean liverworts comprising The description of the underleaf-bearing Brevianthus Plagiochilaceae, Lophocoleaceae and Brevianthaceae hypocanthidium M.A.M. Renner & J.J. Engel (Renner et al. (Hentschel et al. 2006a; He-Nygrén et al. 2006; Engel et al. 2015) further blurred the morphological differences of 2010; Feldberg et al. 2014). This lineage includes succubously Brevianthaceae and Lophocoleaceae. foliated, perianth-bearing liverworts with predominantly Here, we present the most comprehensively sampled phy- polystratose capsule walls. It represents the most speciose logeny for the Brevianthaceae-Lophocoleaceae- clade of suborder Lophocoleineae and may include more than Plagiochilaceae lineage to date. This phylogeny allows us to 1000 species (Söderström et al. 2015, 2016). Most species of explore the monophyly of and relationships between many Plagiochilaceae have reduced underleaves, scattered rhizoids, currently accepted subgenera and genera, with a higher degree undivided leaves and laterally compressed bilabiate perianths of stringency than possible previously. The phylogeny pre- with a truncate mouth (Crandall-Stotler et al. 2009). In terms sents evidence for the polyphyly of Acrochila R.M. Schust., of species numbers, this family is dominated by Plagiochila Plagiochila and Plagiochilion S. Hatt. We discuss different (Dumort.) Dumort., a cosmopolitan genus distinguished by approaches to resolving monophyletic genera, advocate trans- dioicy, alternating (rarely subopposite) foliation and nearly fer of Acrochila and Plagiochilion to Chiastocaulon and in- exclusively lateral branching (Inoue and Schuster 1971; troduce the genus Cryptoplagiochila. Inoue 1984;Heinrichs2002). Several putative satellite genera originally segregated on the basis of their unusual morphology have been identified as elements of Plagiochila based on mo- Material and methods lecular data and a reconsideration of morphological evidence, i.e. Rhodoplagiochila R.M. Schust. (Heinrichs et al. 2004b), DNA extraction, PCR amplification and sequencing Steereochila Inoue, and Szweykowskia Gradst. & M.E. Reiner (Heinrichs 2002). Chiastocaulon Carl (Groth and Heinrichs Plant tissue was isolated from dried herbarium specimens and 2003)andDinckleria Trevis. (Engel and Heinrichs 2008) used to extract genomic DNA with either the Invisorb Spin were reinstated for the same reasons. Plant Mini Kit (Invitek, Berlin) or the Qiagen DNeasy 96 In contrast to the Plagiochilaceae, the Lophocoleaceae have Plant Kit (QIAGEN, Valencia, CA). Sequences were either conspicuous, bifid underleaves, fascicled rhizoids, bifid or generated at Ludwig Maximilians University Munich or at undivided leaves and trigonous perianths with three conspic- the Royal Botanical Gardens Sydney. PCR was conducted uous keels (Hentschel et al. 2006a). The generic classification for the nuclear ribosomal internal transcribed spacer region of the Lophocoleaceae is currently in flux, with two different (nrITS1-5.8S-ITS2, hereafter ITS) and the plastid regions classification systems currently advocated. One is based on a rps4andrbcL. broadly defined genus Chiloscyphus Corda (Engel and Schuster 1984;HässeldeMenéndez1996; Hentschel et al. Munich sequencing protocols PCR and sequencing proto- 2006b), which includes Lophocolea (Dumort.) Dumort. and cols followed Hentschel et al. (2006a)forrbcL, Groth and several putative satellite genera (Hentschel et al. 2007). The Heinrichs (2003)forrps4 and Feldberg et al. (2004)forITS. other system is based on the recognition of Lophocolea,be- Sequencing was carried out on an ABI 3730 capillary se- side a Chiloscyphus reduced to the type species Chiloscyphus quencer using the BigDye Terminator v3.1 Cycle Sequencing polyanthos (L.) Corda and its diploid derivative Chiloscyphus Kit (Applied Biosystems, Foster City, CA, USA). Primers pallescens (Hoffm.) Dumort. (Hentschel et al. 2006b), the used for PCR amplification were also used for sequencing. retention of Pachyglossa Herzog & Grolle, plus a polyphyletic New sequences were assembled and edited in CodonCode genus Clasmatocolea Spruce and the new genus Aligner 5.0.1 (CodonCode Corp., Dedham, MA, USA). Cryptolophocolea L. Söderstr., Crand.-Stotl., Stotler & Váňa (Söderström et al. 2013). Sydney sequencing protocols All reaction volumes were Brevianthaceae was established (Engel and Schuster 1981) 25 μL and contained 17 μL MilliQ water, 2.5 μL10× to accommodate Brevianthus flavus (Grolle) J.J. Engel & Immolase Buffer (Bioline, London), 2 μL 2.5 mM dNTPs, A phylogeny of Lophocoleaceae-Plagiochilaceae-Brevianthaceae 483 1.25 μL50mMMgCl2,0.25μL 0.4 % BSA, 0.5 μL10μM statistically supported (>70 % bootstrap value) contradiction Forward
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