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Phylogeny and Systematics of the Tribe Thlaspideae (Brassicaceae) and the Recognition of Two New Genera Shokouh Esmailbegi,1,2 Ihsan A

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Phylogeny and Systematics of the Tribe Thlaspideae (Brassicaceae) and the Recognition of Two New Genera Shokouh Esmailbegi,1,2 Ihsan A Esmailbegi & al. • Phylogeny and systematics of Thlaspideae (Brassicaceae) TAXON 67 (2) • April 2018: 324–340 Phylogeny and systematics of the tribe Thlaspideae (Brassicaceae) and the recognition of two new genera Shokouh Esmailbegi,1,2 Ihsan A. Al-Shehbaz,3 Milan Pouch,2 Terezie Mandáková,2 Klaus Mummenhoff,4 Mohammad Reza Rahiminejad,1 Mansour Mirtadzadini5 & Martin A. Lysak2 1 Department of Biology, University of Isfahan, Hezarjarib Street, Isfahan 81746-73441, Iran 2 Central European Institute of Technology (CEITEC) and Faculty of Science, Masaryk University, Kamenice 5, 62500 Brno, Czech Republic 3 Missouri Botanical Garden, P.O. Box 299, St. Louis, Missouri 63166-0299, U.S.A 4 Department of Biology, Botany, University of Osnabrück, Barbarastrasse 11, 49076 Osnabrück, Germany 5 Shahid Bahonar University of Kerman, 22 Bahman Blvd., Afzalipour Square, P.O. Box 76169-133, Kerman, Iran Author for correspondence: Martin A. Lysak, [email protected] DOI https://doi.org/10.12705/672.4 Abstract Thlaspideae is an Old World tribe of Brassicaceae centered in SW Asia. Thirty-seven of 42 species (ca. 88%) in 13 genera of the tribe were analyzed using nuclear ITS and chloroplast trnL-F markers in a family-wide context. Both single- marker and concatenated phylogenies corroborated Thlaspideae as a well-supported monophyletic clade. With the exception of polyphyletic Alliaria and Parlatoria and paraphyletic Thlaspi and Didymophysa, the remaining genera were monophyletic. Alliaria petiolata comprised diploid and hexaploid populations in two well-resolved clades. The non-weedy diploid and hexa- ploid populations are restricted to SW Asia, and together with diploid A. taurica (formerly P. taurica), formed a sister clade to well-resolved Sobolewskia (3 spp.) and P. rostrata (now treated as the new monospecific genus Lysakia) clades. By contrast, the European and North American weedy and invasive hexaploid A. petiolata populations clustered with the diploid P. caki- loidea. Polyphyletic Thlaspi formed two distinct clades easily distinguished morphologically, and two of its six species are segregated into the new genus Mummenhoffia. Elburzia is reduced to synonymy of Didymophysa, and the new combinations D. fenestrata, Lysakia rostrata, Mummenhoffia alliacea, and M. oliveri are proposed and a diagnostic key for determination of Thlaspideae genera is presented. Age estimations based only on calibration by the controversial fossil Thlaspi primeavum resulted in unrealistic old age estimates. Chromosome counts are reported for 16 species. Keywords Alliaria; chromosome counts; Cruciferae; Didymophysa; Elburzia; Lysakia; Mummenhoffia; Parlatoria; phylogeny; taxonomy; Thlaspideae Supplementary Material The Electronic Supplement (Tables S1, S2; Figs. S1–S3; Appendix S1) and DNA sequence alignment are available from https://doi.org/10.12705/672.4.S1 and https://doi.org/10.12705/672.4.S2, respectively. INTRODUCTION 2011; Mohammadin & al., 2017) have proposed that it might have been the cradle of the family. The age estimate of the The Brassicaceae (Cruciferae, or mustard family) include family is not fully settled because some (e.g., Beilstein & al., some 3980 species in 351 genera of 52 tribes (BrassiBase, 2017; 2010) suggested an Eocene origin (ca. 54 Ma), whereas most Kiefer & al., 2014). It is of a special interest because it includes other authors suggested a younger origin in the Late Oligocene, many vegetable crops (e.g., Brassica oleracea L., B. rapa L., with the major diversification ca. 25 Ma in the Miocene (e.g., Raphanus sativus L.), ornamentals (e.g., Arabis L., Aubrieta Franzke & al., 2009, 2011, 2016; Salariato & al., 2016; Guo & Adans., Erysimum L., Iberis L., Lunaria L.), condiments al., 2017; Lopez & al., 2017). (Armoracia rusticana G. Gaertn. & al., Eutrema japonicum The tribal classifications of the Brassicaceae pre-dating the (Miq.) Koidz., Sinapis alba L.), vegetable oils such as canola era of molecular systematics (e.g., Candolle, 1821a, b; Prantl, (B. napus L.), numerous weeds, and several model plants, such 1891; Hayek, 1911; Schulz, 1936) were artificial because de- as Arabidopsis thaliana (L.) Heynh. (Franzke & al., 2011). limitation of tribal boundaries was based on morphological The family is distributed on all continents except characters that were subject to considerable convergence during Antarctica, and it is particularly abundant in the temperate and the evolutionary history of the family (Franzke & al., 2011). alpine areas of the world, with the major distribution centers in Al-Shehbaz & al. (2006) introduced the first phylogenetic clas- the Irano-Turanian region, Mediterranean region, and western sification of the family primarily based on molecular phyloge- North America (Hedge, 1976; Appel & Al-Shehbaz, 2003; Al- netic studies by Beilstein & al. (2006). The original 25 tribes Shehbaz & al., 2006). Turkey has the highest concentration of (Al-Shehbaz & al., 2006) went up to 49 (Al-Shehbaz, 2012) and native crucifers in any country, and some (e.g., Franzke & al., to 52 most recently (Kiefer & al., 2014). Article history: Received: 21 Sep 2017 | returned for (first) revision: 20 Nov 2017 | (last) revision received: 6 Dec 2017 | accepted: 12 Dec 2017 | published: online fast track, n/a; in print and online issues, 9 May 2018 || Associate Editor: Alessia Guggisberg || © International Association for Plant Taxonomy (IAPT) 2018, all rights reserved 324 Version of Record TAXON 67 (2) • April 2018: 324–340 Esmailbegi & al. • Phylogeny and systematics of Thlaspideae (Brassicaceae) Some of the Brassicaceae tribes were subjected to more recent attempted to utilize the molecular data to resolve the taxonomy molecular studies, and the relationships of their component gen- of problematic genera such as Alliaria, Didymophysa, Elburzia, era are fairly well understood. These include the tribes (and latest Parlatoria, and Thlaspi. reference) Aethionemeae (Mohammadin & al., 2017), Alysseae (Španiel & al., 2015), Anchonieae and Euclidieae (Warwick & al., 2007; Jaén-Molina & al., 2009), Aphragmeae (Warwick & al., MATERIALS AND METHODS 2006a), Arabideae (Karl & Koch, 2013), Biscutelleae (Özüdoğru & al., 2017), Boechereae (Alexander & al., 2013), Brassiceae (Arias Taxon sampling. — Samples for the molecular studies in- & al., 2014), Chorisporeae (German & al., 2011), Cochlearieae cluded silica-gel dried leaves collected during fieldwork mainly (Koch, 2012), Coluteocarpeae (Firat & al., 2014), Cremolobeae in Iran (with a few samples of Alliaria petiolata (M.Bieb.) (Salariato & al., 2013), Descurainieae (Goodson & al., 2011), Cavara & Grande from Austria, Czech Republic, and France), Erysimeae (Moazzeni & al., 2014), Eudemeae (Salariato & al., fresh leaf material from plants grown from seeds, and tiny frag- 2015), Eutremeae (Warwick & al., 2006a), Halimolobeae (Bailey ments taken from herbarium specimens deposited at FUMH, & al., 2007), Heliophileae (Mummenhoff & al., 2005), Lepidieae G, HUB, Isfahan (Isfahan University herbarium, Iran), LE, (Mummenhoff & al., 2009), Microlepidieae (Mandáková & Lysak (Martin A. Lysak private herbarium, Czech Republic), al., 2017), Physarieae (Fuentes-Soriano & Al-Shehbaz, 2013), M, MIR, MO, MSB, PR, Sanandaj (Herbarium of Kurdistan, Schizopetaleae and Thelypodieae (Cacho & al., 2014; Toro- Iran), W, and WU. Vouchers of all samples collected by the first Núñez & al., 2014), Sisymbrieae (Warwick & al., 2006b), and author are deposited in MIR, MO, and W. In total, 91 acces- Smelowskieae (Warwick & al., 2004). The Cardamineae and sions from 37 of the 42 Thlaspideae species of 13 genera were Thlaspideae are among some of the most widespread tribes that included in the analyses, representing the full range of morpho- have not been subjected to critical molecular phylogenetic and logical variation and the entire geographic distribution of the systematics studies. tribe. Graellsia chitralensis O.E.Schulz, G. hissarica Junussov, Although the tribe Thlaspideae was initially proposed by Pseudocamelina conwayi (Hemsl.) Al-Shehbaz, and Thlaspi Candolle (1821a), it was not recognized by subsequent authors kochianum F.K.Mey. are known only from the type collections except for Prantl (1891). Of the initial 87 species recognized and, therefore, were not included in the study. Furthermore, by Candolle (1821b), only 3 of 17 species of Thlaspi L. (i.e., Pseudocamelina campylopoda was not included due to the T. alliaceum L., T. arvense L., T. ceratocarpum Murr.) are cur- insufficient quality of DNA isolated from its three accessions. rently maintained in the tribe (Meyer, 2001). The other genera In addition, sequence data of 13 species in 10 Thlaspideae gen- of Thlaspideae accepted by Candolle included Biscutella L. era were taken from GenBank. To examine the monophyly of (Biscutelleae), Capsella Medik. (now in tribe Camelineae), Thlaspideae, 22 species of 16 Brassicaceae tribes in lineage II Cremolobus DC. and Menonvillea DC. (both Cremolobeae), and expanded lineage II were used, and the outgroup included illegitimate Hutchinsia W.T.Aiton (now Hornungia Rchb. of three species of three tribes of lineage III Appendix 1). For Descurainieae), Megacarpaea DC. (Megacarpaeeae), and component tribes of all lineages, see Kiefer & al. (2014). Teesdalia W.T.Aiton and Iberis L. (both Iberideae). The genera DNA extraction. — Total DNA was extracted using Alliaria Heist. ex Fabr., Peltaria Jacq., and Sobolewskia M.Bieb., either the modified CTAB method (Doyle & Doyle, 1987) which are currently accepted in Thlaspideae (Al-Shehbaz,
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