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Phylogenetic Relationships in Nartheciaceae (Dioscoreales), with Focus on Pollen and Orbicule Morphology

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Phylogenetic Relationships in Nartheciaceae (Dioscoreales), with Focus on Pollen and Orbicule Morphology Belg. J. Bot. 141 (1) : 64-77 (2008) © 2008 Royal Botanical Society of Belgium PHYLOGENETIC RELATIONSHIPS IN NARTHECIACEAE (DIOSCOREALES), WITH FOCUS ON POLLEN AND ORBICULE MORPHOLOGY Vincent MERCKX1,*, Peter SCHOLS1, Koen GEUTEN1,2, Suzy HUYSMANS1 and Erik SMETS1,3 1 Laboratory of Plant Systematics, K.U.Leuven, Kasteelpark Arenberg 31, P.O. Box 2437, B-3001 Leuven, Belgium 2 Department of Molecular, Cellular and Developmental Biology, Yale University, New Haven, USA 3 National Herbarium of the Netherlands, Leiden University Branch, P.O. Box 9514, 2300 RA Leiden, the Netherlands (* Author for correspondence; e-mail: [email protected]) Received 4 May 2007; accepted 24 September 2007. ABSTRACT. — A molecular phylogenetic analysis of Nartheciaceae is presented, with nine species of the family’s five genera. The main phylogenetic findings are: (a) Nietneria and Narthecium are placed in a clade sister to Lophiola; (b) sister to the Lophiola-Narthecium- Nietneria clade is a clade formed by Aletris and the monospecific Metanarthecium; (c) the inclusion of Metanarthecium luteo-viride in Aletris, as proposed by several authors, is well supported. The pollen and orbicule morphology of representatives of five genera is described. The results underline a close relationship between Nietneria, Narthecium, and Lophiola and confirm the previously reported observations of Metanarthecium pollen and the types of sex- ine ornamentation in Aletris. Pollen grains of Nietneria are monosulcate with a microreticulate sexine, confirming a close relationship with Lophiola and Narthecium. Spherical smooth- surfaced orbicules were observed in all genera of Nartheciaceae and the presence of a circular perforation on the orbicule surface is potentially synapomorphic for the family. KEY WORDS. — Dioscoreales, Nartheciaceae, Nietneria, molecular phylogeny, orbicules, pollen morphology. INTRODUCTION of North America, Europe and Asia, but is absent from China (TAMURA 1998). Lophiola Ker Gawl. The family Nartheciaceae Fr. ex Bjurzon (one species), easily recognizable by its whitish comprises five genera (CADDICK et al. 2002a). woolly inflorescence, grows in acid, pine barren Nartheciaceae are perennial herbs with short bogs from New Jersey to Florida and Nova Sco- tuberculate or creeping rhizomes, erect stems and tia. In some treatments more than one Lophiola terminal spikes or racemes. They occur mostly in species are recognized based on morphological wet habitats, such as swamps and bogs (TAMURA differences between specimens from different 1998). Aletris L. (ca. 33 species) is the largest populations (ROBERTSON 1976, DAHLGREN et al. genus of Nartheciaceae, with representatives in 1985, TAMURA 1998). This morphological varia- Eastern Asia and North America (TAMURA 1998). tion may be due to ecological conditions Narthecium Huds. (ca. eight species) has a dis- (ROBERTSON 1976, ZAVADA et al. 1983, AMBROSE junct distribution and occurs in temperate regions 1985). Lophiola was previously linked with PHYLOGENETIC RELATIONSHIPS IN NARTHECIACEAE 65 Lachnanthes Elliot and placed in Haemodoraceae 1998). As a result, Narthecium, Aletris, Meta- (GEERINCK 1969, HUTCHINSON 1973, ORNDUFF narthecium, Lophiola and Nietneria were linked 1979). However, this position proved to be incor- with Tofieldia, Pleea, Isidrogalvia, Harperocal- rect (SIMPSON 1981, SIMPSON & DICKISON 1981, lis, Japanolirion and the saprophytic genus Pet- ZAVADA et al. 1983) and based on several mor- rosavia (AMBROSE 1980, TAMURA 1998). phological characters Lophiola was transferred to DAHLGREN et al. (1985) also included Heloniop- Nartheciaceae (AMBROSE 1980, 1985, GOLDBLATT sis, Helionas and Ypsilandra together with the 1995, ZOMLEFER 1997, 1999), a placement later five Nartheciaceae genera of the present treat- confirmed by the molecular analyses of CADDICK ment in a tribe Narthecieae, in the family Melan- et al. (2000, 2002b), FUSE & TAMURA (2000) and thiaceae. Several recent molecular analyses inde- TAMURA et al. (2004). Nietneria Klotzsch & pendently indicated that Nartheciaceae are related R.Schomb. is restricted to savannas from high- to Burmanniaceae and Dioscoreaceae, and there- lands of Venezuela and Guyana. Two Nietneria fore, the family should be included in Dioscore- species are delimited (FRAME 2004, MAAS & ales (APG I 1998, CADDICK et al. 2000, CHASE et WESTRA 2005), but some authors recognize only al. 2000, FUSE & TAMURA 2000, CADDICK et al. one species (DAHLGREN et al. 1985, TAMURA 2002b, APG II 2003, TAMURA et al. 2004, CHASE 1998). The fifth genus of Nartheciaceae, Meta- et al. 2006, GIVNISH et al. 2006, MERCKX et al. narthecium Maxim., contains a single species, M. 2006). luteo-viride, which is endemic to Japan where it Some of the studies mentioned above also grows in subalpine meadows. Recently, some give an indication of intergeneric relationships in authors included M. luteo-viride in Aletris, on the Nartheciaceae. In the analyses of CADDICK et al. basis of morphological similarities and a shared (2002b), FUSE & TAMURA (2000) and TAMURA et basic chromosome number, x = 13 (TAMURA al. (2004), Lophiola and Narthecium form a clade 1998, ZOMLEFER 1999). This was supported by with high bootstrap support, although in these the combined molecular and morphological studies only one species from each genus was analysis of CADDICK et al. (2002b), which sampled. In the combined molecular (rbcL, atpB grouped Metanarthecium with Aletris farinosa and 18S rDNA) and morphological study of CAD- with high bootstrap support. However, the molec- DICK et al. (2002b) the Lophiola-Narthecium ular analysis of FUSE & TAMURA (2000) and clade was sister to a strongly supported Aletris TAMURA et al. (2004) placed Metanarthecium sis- farinosa-Metanarthecium luteo-viride clade. This ter to Narthecium and Lophiola, with no boot- contradicted the analyses of FUSE & TAMURA strap support. TAMURA et al. (2004) presented evi- (2000) based on matK sequence data. Their dence for the inclusion of Isidrogalvia Ruiz & results placed Metanarthecium as sister to Lophi- Pav. (Tofieldiaceae) in Nartheciaceae. In their ola and Narthecium instead of Aletris. Nietneria combined matK-rbcL strict consensus tree Isidro- was not incorporated in any molecular study. galvia schomburgkiana was sister to Narthecium Although Dioscoreales are clearly defined with maximum bootstrap support. Isidrogalvia, in recent molecular studies, their morphology is which is indigenous to South America, consists of heterogeneous. Recent morphological research in six species (CRUDEN 1991, CRUDEN & DORR Dioscoreales focused mainly on microsporogene- 1992). However, a recent study with matK data on sis and pollen morphology (CADDICK et al. 1998, a broad Tofieldiaceae sampling, including three SCHOLS et al. 2001, 2003). These morphological Isidrogalvia species, confirmed the placement of features provided taxonomically useful charac- Isidrogalvia in Tofieldiaceae with maximal boot- ters, particularly at the genus level. SCHOLS et al. strap support (AZUMA & TOBE 2005). (2001, 2003) showed that pollen characters are The circumscription and affinities of the valuable for delimiting sections within Dioscorea family have been subject to change. Most authors (Dioscoreaceae) and are, moreover, highly con- previously included the genera of Nartheciaceae gruent with molecular data (SCHOLS et al. 2005). in a broadly defined Melanthiaceae (TAMURA CADDICK et al. (1998) studied microsporogenesis 66 BELGIAN JOURNAL OF BOTANY 141 and pollen morphology in Dioscoreales and allied MATERIALS AND METHODS taxa. They concluded that ‘both microsporogene- sis and pollen morphology provide characters We inferred the intergeneric relationships of which are taxonomically useful at the genus level, Nartheciaceae using sequences from the plastid atpB- especially in Dioscoreaceae and its close allies, rbcL spacer, the trnL intron and trnL-trnF intergenic but probably less informative at higher taxonomic spacer region. We selected these particular noncoding DNA regions because they evolve relatively rapidly levels, although this has yet to be tested in mor- and are, therefore, effective in resolving phylogenetic phological and combined morphological-molecu- questions at the genus level (e.g. MANEN & NATALI lar analyses’ (p. 329). Since these and previous 1996, CHANDERBALI et al. 2001). In addition the studies contained an incomplete sampling of nuclear 18S rDNA region was sequenced for all sam- Nartheciaceae, we examined the pollen morphol- ples. This generally conservative DNA region has ogy of representatives of five genera of Nartheci- proven to be very useful for phylogeny inference in aceae. Previous pollen morphological observa- Dioscoreales (CADDICK et al. 2002b, MERCKX et al. tions of Nartheciaceae were published by ZAVADA 2006). Our sampling includes species of all genera of et al. (1983), TAKAHASHI & KAWANO (1989) and Nartheciaceae. Lophiola specimens from two different CADDICK et al. (1998). According to their results populations, one from Florida and one from Nova Sco- the pollen grains of Lophiola, Narthecium, Meta- tia, are present. In order to distinguish these specimens, we labelled the specimen from Nova Scotia as L. amer- narthecium and Aletris are monosulcate and sex- icana. According to most authors L. americana is a ine ornamentation varies from microreticulate in synonym of L. aurea (ROBERTSON 1976, ZAVADA et al. Narthecium and Lophiola, reticulate in Meta- 1983, AMBROSE 1985). Since Dioscoreaceae and Bur- narthecium to perforate, reticulate and gemmate
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