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Two New Genera in the Omphalodes Group (Cynoglosseae, Boraginaceae)

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Two New Genera in the Omphalodes Group (Cynoglosseae, Boraginaceae) Nova Acta Científica Compostelana (Bioloxía),23 : 1-14 (2016) - ISSN 1130-9717 ARTÍCULO DE INVESTIGACIÓN Two new genera in the Omphalodes group (Cynoglosseae, Boraginaceae) Dous novos xéneros no grupo Omphalodes (Cynoglosseae, Boraginaceae) M. SERRANO1, R. CARBAJAL1, A. PEREIRA COUTINHO2, S. ORTIZ1 1 Department of Botany, Faculty of Pharmacy, University of Santiago de Compostela, 15782 Santiago de Compostela , Spain 2 CFE, Centre for Functional Ecology, Department of Life Sciences, University of Coimbra, 3000-456 Coimbra, Portugal *[email protected]; [email protected]; [email protected]; [email protected] *: Corresponding author (Recibido: 08/06/2015; Aceptado: 01/02/2016; Publicado on-line: 04/02/2016) Abstract Omphalodes (Boraginaceae, Cynoglosseae) molecular phylogenetic relationships are surveyed in the context of the tribe Cynoglosseae, being confirmed that genusOmphalodes is paraphyletic. Our work is focused both in the internal relationships among representatives of Omphalodes main subgroups (and including Omphalodes verna, the type species), and their relationships with other Cynoglosseae genera that have been related to the Omphalodes group. Our phylogenetic analysis of ITS and trnL-trnF molecular markers establish close relationships of the American Omphalodes with the genus Mimophytum, and also with Cynoglossum paniculatum and Myosotidium hortensia. The southwestern European annual Omphalodes species form a discrete group deserving taxonomic recognition. We describe two new genera to reduce the paraphyly in the genus Omphalodes, accommodating the European annual species in Iberodes and Cynoglossum paniculatum in Mapuchea. The pollen of the former taxon is described in detail for the first time. Keywords: Madrean-Tethyan, phylogeny, pollen, systematics, taxonomy Resumo Neste estudo analisamos as relacións filoxenéticas deOmphalodes (Boraginaceae, Cynoglosseae) no contexto da tribo Cynoglosseae, confirmándose como parafilético o xéneroOmphalodes . Neste traballo colocamos o foco tanto nas relacións internas entre diversos representantes dos principais subgrupos dentro de Omphalodes (e incluíndo Omphalodes verna, a especie tipo), como nas relacións destes con outros xéneros das Cynoglosseae que teñen sido relacionados co grupo Omphalodes. A nosa análise filoxenética cos marcadores moleculares ITS etrn L-trnF estabelece a proximidade entre as Omphalodes americanas e o xénero Mimophytum, así como con Cynoglossum paniculatum e Myosotidium hortensia. As Omphalodes anuais do suroeste europeo forman un grupo característico merecedor de recoñecemento taxonómico. Describimos dous novos xéneros para reducir a parafília do xénero Omphalodes, acomodando as especies europeas anuais en Iberodes e Cynoglossum paniculatum en Mapuchea. O pólen deste último taxón é descrito en pormenor por vez primeira. Palabras chave: Madreano-Tetiano, filoxenia, pólen, sistemática, taxonomía INTRODUCTION related to a generic trend to nutlets comparatively bigger than gynobasis (BRAND, 1921). Beside The genus Omphalodes Moench (1794: 419) that, the most defining trait of Omphalodes is (Boraginaceae) comprises ca. 25 annual, biennial dorsally compressed nutlets with a wing circling and perennial herbaceous species mostly from the margins of the upper side. Published molecular temperate habitats of the northern hemisphere. The phylogenies (WEIGEND et al. 2013) and our own distribution of the genus showed a striking dis- previous results (see COUTINHO et al., 2012) junct range, with three separate groups of species have revealed unsuspected close relationships of occurring in North America (Mexico and Texas), Omphalodes with two taxa, Myosotidium hortensia Western Eurasia and the Japanese archipelago, but Baillon (1890: 383) and Cynoglossum paniculatum the Japanese species were recently accommodated Hook. & Arn. (1830: 37). The former is a shrub in the new genus Nihon (OTERO et al., 2014). As species occurring in the Chatham archipelago in a result, Omphalodes as is now recognized appears New Zealand, very different to Omphalodes both to fit relatively well to the Madrean-Tethyan Flora in terms of habit and inflorescence but in fruit biogeographical pattern (RAVEN & AXELROD, features resembles Omphalodes, being somewhat 1974; WEN & ICKERT-BOND, 2009), a disjunct winged nutlets and an expanded scar. The latter pattern of species distribution between the Medite- is a Chilean endemic that was considered a mem- rranean areas in Eurasia and North America. ber of the core Cynoglossum group by BRAND The internal systematics of Boraginaceae have (1921). This species has unwinged nutlet covered payed particular attention to fruit morphological by glochidiate hooks, a typical feature of the characters to establish distinctions among and genus Cynoglossum (JOHNSTON, 1924, 1927), within tribes, being Omphalodes traditionally but that is also present in a number of taxa of the recognized as a member of the tribe Cynoglos- Cynoglosseae (i.e. Trichodesma, Lappula, ...). seae (DE CANDOLLE, 1846; JOHNSTON, 1924; Since Myosotidium hortensia and Cynoglossum POPOV, 1953; RIEDL, 1997). The Cynoglosseae paniculatum are recovered among the Omphalodes show great variation in external fruit morphol- in the phylogenetic works cited above, the genus ogy, and therefore the traditional systematics of as currently circumscribed is paraphyletic. In this the tribe heavily relied on few relatively constant work we want firstly to explore the phylogenetic traits, mainly gynobase shape and apical attach- relationships, based both on plastid (trnL-trnF ment scar position in the nutlet (JOHNSTON, spacer) and nuclear (ITS1+5.8S+ITS2 region) 1924; RIEDL, 1997). However LÅNGSTRÖM molecular markers of Omphalodes and Cynoglos- & CHASE (2002) molecular phylogenies sug- sum paniculatum with other possibly close genera gested that the Cynoglosseae should be merged in family-wide phylogenetic analysis. with other tribes (LÅNGSTRÖM & OXELMAN, Secondly, we want to clarify the identity of 2003; WEIGEND et al., 2010; NAZAIRE & HUF- two conspicuous groups of Omphalodes, the FORD, 2012; WEIGEND et al., 2013; OTERO et Mexican-Texan group and the south-western Eu- al., 2014), among them the large tribe Eritrichieae, ropean annual taxa group. Regarding the former, morphologically defined by having a nutlet at- possible relationships with genus Mimophytum tachment scar in a basal position (JOHNSTON, Greenm. (1905: 242) have to be suerveyed. This 1924; AL-SHEHBAZ, 1991; RIEDL, 1997). genus is a member of the Cynoglosseae of which These results gave final support to previous con- habit similarities with Mexican Omphalodes siderations that Cynoglosseae systematics based have been highlighted, in spite of its glochidiate on fruit morphology could be rather artificial fruit (GREENMAN, 1905; JOHNSTON, 1924). (AL-SHEHBAZ, 1991). In this context, the genus In this sense, recently, Omphalodes richardsonii Omphalodes never accommodated well in terms Nesom 1988:27, the only previously Omphal- of the attachment scar to the Cynoglosseae or the odes described species with slightly glochid-like Eritrichieae, having big scars covering a great part appendages in fruit has been transferred to the of the inner side of the nutlet (POPOV, 1953) that hitherto monotypic genus Mimophytum (Mimo- hardly can be considered apical. This feature can be phytum richardsonii (Nesom 1988: 27) NESOM, 2013: 9). Regarding the European annuals, it 5’-GGAAGGAGAAGTCGTAACAAGG-3’. must be noted that the annual species of south PCR reactions were performed using Ready-To-Go western Europe form a well identified group PCR beads (GE Healthcare) in a Thermo Electron of taxa (POPOV, 1953; GRAU, 1967). , being PXE 0,2 thermal cycler. PCR conditions were an Omphalodes aliena A. Gray ex Hemsley (1882: initial denaturation of 94 º C for 3-4 min, followed 377) and Omphalodes alienoides G.L. Nesom by 35 cycles of 94 ºC denaturation for 1-2 min, (2013: 10), two Texan-Mexican species closely 46-53 º C annealing for 1 min and 71 º C extension related between them, the only two other annual for 1-5 min sec. Sequencing was performed in an (sometimes biennal) taxa in the genus. Identity automated DNA sequencer (Model 377, Applied and possible relationships between these groups Biosystems). are also surveyed. And thirdly, in order to have a Automatic alignments were conducted by Ge- more natural classification, we will propose new neious (Geneious 7.1.4, created by Biomatters. genera, supported by the molecular phylogeny Available from http://www.geneious.com/ ) and giving morphological and palynological and followed by manual analysis in BioEdit information of the characteristic features of the (HALL, 1999). The complete data set had 1277 genera, to accommodate the nomenclature to the aligned positions, of which 763 belonged to the evolutionary relationships. ITS1+5.8S+ITS2 region and 514 to the trnL-trnF. PartitionFinder (LANFEAR et al., 2012) was used for selecting best-fit partitioning schemes MATERIAL AND METHODS and models of molecular evolution using both the “greedy” and “all” algorithms. Four representa- Phylogenetic analysis tives of the order Boraginales belonging to the Cordiaceae, Hydrophyllaceae and Heliotropiaceae Plant material used in the phylogenetic analy- families were used as outgroup (Table I). Maxi- sis derives from field collections or herbarium mum Likelihood phylogenetic analyses were run sheets. The ingroup dataset included Myosotidium in RAxML (STAMATAKIS et al., 2008). Three hortensia, Mimophytum omphalodoides and subset
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