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Phylogeny and Generic Delimitation in Molluginaceae, New Pigment Data in Caryophyllales, and the New Family Corbichoniaceae Mats Thulin,1 Abigail J

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Phylogeny and Generic Delimitation in Molluginaceae, New Pigment Data in Caryophyllales, and the New Family Corbichoniaceae Mats Thulin,1 Abigail J TAXON 65 (4) • August 2016: 775–793 Thulin & al. • Phylogeny of Molluginaceae Phylogeny and generic delimitation in Molluginaceae, new pigment data in Caryophyllales, and the new family Corbichoniaceae Mats Thulin,1 Abigail J. Moore,2 Hesham El-Seedi,3,4 Anders Larsson,1 Pascal-Antoine Christin5 & Erika J. Edwards2 1 Systematic Biology, EBC, Uppsala University, Norbyvägen 18D, 752 36 Uppsala, Sweden 2 Department of Ecology and Evolutionary Biology, Brown University, 80 Waterman St, Box G-W, Providence, Rhode Island 02912, U.S.A. 3 Division of Pharmacognosy, BMC, Uppsala University, Box 574, 751 23 Uppsala, Sweden 4 Department of Chemistry, University of Malaya, 50603 Kuala Lumpur, Malaysia 5 Department of Animal and Plant Sciences, University of Sheffield, Western Bank, Sheffield S10 2TN, U.K. Author for correspondence: Mats Thulin, [email protected] ORCID PAC, http://orcid.org/0000-0001-6292-8734 DOI http://dx.doi.org/10.12705/654.6 Abstract The circumscription of Molluginaceae has changed radically in recent years, with Corbichonia being moved to Lophiocarpaceae, Limeum to Limeaceae, Macarthuria to Macarthuriaceae and all species of Hypertelis, except the type, to Kewa in Kewaceae. In a broad analysis of core Caryophyllales using plastid trnK-matK and rbcL sequences, the position of Molluginaceae in a strict sense as sister to the Portulacineae clade is corroborated, as are the positions of Corbichonia, Limeum and Kewa outside the family. The phylogeny of Molluginaceae is reconstructed based on trnK-matK and nuclear ITS sequences of about half of the currently recognized species in the family and with representatives from all recognized genera. Mollugo is found to be polyphyletic and a new taxonomy for the family with 11 genera is proposed. Mollugo in its new restricted sense is a mainly American genus of about 15 species, including M. ulei comb. nov., previously placed in the monotypic Glischrothamnus. The Australian and Asian genus Trigastrotheca is resurrected for T. molluginea, T. pentaphylla comb. nov. and T. stricta comb. nov. The name Paramollugo nom. nov. is proposed for the Mollugo nudicaulis group and the combinations P. angustifolia comb. nov., P. cuneifolia comb. nov., P. decandra comb. nov., P. deltoidea comb. nov., P. navas- sensis comb. nov. and P. nudicaulis comb. nov. are made. Hypertelis is expanded to include, besides the type H. spergulacea, also H. cerviana comb. nov., H. fragilis comb. nov., H. umbellata comb. nov. and H. walteri comb. nov. In Pharnaceum, the new combination P. namaquense comb. nov. is made, Hypertelis longifolia is treated as a synonym of P. lineare and Mollugo tenella as a synonym of P. subtile. Corbichonia is proposed to be treated as a family of its own, Corbichoniaceae fam. nov. Several names are lectotypified, including the Linnaean Mollugo pentaphylla and M. stricta. An anthocyanin is reported for the first time from Simmondsiaceae. The detection of anthocyanins in members of Kewaceae and Molluginaceae agree with previous reports and corroborate the view that these families represent reversals from betalains to anthocyanins. The report of an anthocyanin in Limeaceae, previously regarded as unpigmented, apparently represents a newly detected reversal from betalains to anthocyanins in this family. Keywords anthocyanins; betalains; Corbichonia; Hypertelis; ITS; Mollugo; Paramollugo; taxonomy; Trigastrotheca; trnK-matK; typification Supplementary Material The Electronic Supplement (Figs. S1–S11) is available in the Supplementary Data section of the online version of this article at http://www.ingentiaconnect.com/content/iapt/tax; DNA sequence alignment is available from TreeBASE (http://purl.org/phylo/treebase/phylows/study/TB2:S18909) INTRODUCTION as Aizoaceae and most other families of Caryophyllales. In­ stead they had anthocyanins as Caryophyllaceae, which led to Mollugo L. and its relatives were long treated as members the view that Molluginaceae and Caryophyllaceae are a pair of Aizoaceae, an early exception being Hutchinson (1926), of closely related families (e.g., Mabry, 1977). who recognized Molluginaceae as distinct from Aizoaceae. In the overview of Molluginaceae by Endress & Bit­ However, the family Molluginaceae was not generally rec­ trich (1993), 13 genera were included in the following or­ ognized until the later part of the 20th century, when it was der: Corbichonia Scop., Limeum L., Macarthuria Hügel ex demonstrated that some of its members did not have betalains Endl., Psammotropha Eckl. & Zeyh., Adenogramma Rchb., Received: 31 Dec 2015 | returned for (first) revision: 15 Feb 2016 | (last) revision received: 4 Mar 2016 | accepted: 4 Mar 2016 || publication date(s): online fast track, n/a; in print and online issues, 30 Aug 2016 || © International Association for Plant Taxonomy (IAPT) 2016 Version of Record 775 Thulin & al. • Phylogeny of Molluginaceae TAXON 65 (4) • August 2016: 775–793 Glischrothamnus Pilger, Mollugo, Glinus L., Hypertelis E.Mey. at least one representative of all recognized genera. Eighty ex Fenzl, Pharnaceum L., Suessenguthiella Friedrich, Coelan- sequences were newly generated for this study, including in thum E.Mey. ex Fenzl and Polpoda C.Presl. Endress & Bittrich particular part of the nuclear ribosomal DNA (ITS). (1993) regarded the anthocyanin-producing Molluginaceae as DNA extraction, amplification and sequencing. — Dried an early branch within Caryophyllales “as betalains must be leaf material (2–10 mg) from herbarium specimens was considered as an advanced character common to most families used for DNA extraction. Samples were extracted using the of the order”. FastDNA SPIN kit (MP Biomedicals, Santa Ana, California, The molecular phylogenies that have appeared since the U.S.A.) following manufacturer’s protocol except that two early 1990s (e.g., Cuénoud & al., 2002; Brockington & al., elution steps were generally used, with 50 µl of DES each 2009, 2011; Christin & al., 2011) have led to a radically changed time to maximize yield. view of the circumscription of Caryophyllales, as well as of the The nuclear ribosomal internal transcribed spacer (ITS) circumscription of Molluginaceae and of its position within and chloroplast trnK-matK regions were amplified using PCR. Caryophyllales. Currently available evidence indicates that Mol­ The primers ITS4 and ITS5 (White & al., 1990) were used to luginaceae is sister to the Portulacineae clade within the core amplify the ITS region, while various combinations of the for­ Caryophyllales and nested among betalain-producing families. ward primers trnKmatK_For H, M, G, and K and the reverse Of the genera listed above for Molluginaceae, Corbichonia has primers trnKmatK_Rev B, C, E, and I, all from Christin & al. been moved to Lophiocarpaceae, Limeum to Limeaceae, Macar- (2011), except for trnKmatK_M (5′-ACTATGTATCATTGGT thuria to Macarthuriaceae, and all species of Hypertelis, except TAAGC-3′). The same PCR protocol was used for both regions, the type, to Kewaceae (Christenhusz & al., 2014). in 25 µl reactions including 1 unit GoTaq (Promega Corpora­ Within Molluginaceae, the results of Christin & al. (2011) tion, Madison, Wisconsin, U.S.A.), 5× GoTaq Reaction Buffer strongly indicated that taxonomic changes are needed, particu­ (Promega), 0.5 mM MgCl2, 0.15 mM each dNTP (New England larly regarding the apparently grossly polyphyletic Mollugo. As Biolabs, Ipswich, Massachusetts, U.S.A.), 0.2 µM each primer, for pigment data, Brockington & al. (2011) stated that the claim and approximately 0.6 ng extracted DNA. The following PCR that Molluginaceae is an anthocyanic family “is not supported program was used: initial denaturation of 3 min at 94°C; 37 by any published data”. The presence of anthocyanins in Mol- cycles of 1 min denaturation at 94°C, 30 s annealing at 48°C lugo (Mears, 1976) “was reported with no reference to experi­ or 51°C, 60 to 150 s extension at 72°C, and final extension of mental data” (Brockington & al., 2011), and the same applies 10 min at 72°C. to the report of anthocyanins in Pharnaceum (Clement & al., PCR products were cleaned with the Exo-SAP PCR Prod­ 1994). Otherwise, within Caryophyllales, the reports of antho­ uct Pre-Sequencing Kit (USB Corporation, Cleveland, Ohio, cyanins in species of Hypertelis now placed in Kewa Christenh. U.S.A.). Cleaned PCR products were sequenced at the Rhode in Kewaceae are surrounded by some doubt (Brockington & Island Genomics and Sequencing Center with either a 3130XL al., 2011), Limeum in Limeaceae is regarded as apparently un­ Genetic Analyzer or a 3500XL Genetic Analyzer (Applied pigmented (Behnke & al., 1983), and some families, such as Biosystems, Life Technologies, Grand Island, New York, Simmondsiaceae, have not been examined for their pigments U.S.A.). The same primers were used for PCR and sequenc­ (Brockington & al., 2011). Brockington & al. (2015) showed ing, with additional internal primers being used to sequence that a single origin of betalain pigmentation in Caryophyllales samples for which trnK-matK could be amplified as a single is most likely and that, accordingly, anthocyanin-producing fragment. Chromatograms were edited and contigs were con­ groups within the betalain clade are to be interpreted as evo­ structed using ChromasPro v.1.7.5 (Technelysium, Tewantin, lutionary reversals. Queensland, Australia). The first aim of the present paper is to investigate the Sequence alignment and phylogenetic analyses. — Se­ phylogenetic position and structure of Molluginaceae with a quences were aligned using MUSCLE v.3.5
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