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Phylogeny and Generic Delimitation of Asian Marantaceae

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Phylogeny and Generic Delimitation of Asian Marantaceae Botanical Journal of the Linnean Society, 2009, 159, 381–395. With 3 figures Phylogeny and generic delimitation of Asian Marantaceae PIYAKASET SUKSATHAN1,2, MATS H. GUSTAFSSON1 and FINN BORCHSENIUS1* 1Department of Biological Sciences, Aarhus University, Ny Munkegade, Building 1540, DK-8000, Downloaded from https://academic.oup.com/botlinnean/article/159/3/381/2418341 by guest on 02 October 2021 Aarhus C, Denmark 2Current address: Queen Sirikit Botanic Garden, P.O. Box 7, Mae Rim, Chiang Mai 50180, Thailand Received 29 August 2008; accepted for publication 3 December 2008 Eight genera and approximately 55 species of Marantaceae occur in Asia. Until recently these were the most poorly understood members of the family, but over the last few years much progress have been made in understanding their alpha taxonomy and distribution. Generic delimitation and phylogenetic relationships between genera, however, remain unclear. We analysed phylogenetic relationships in Asian Marantaceae using maximum parsi- mony and Bayesian analysis of plastid (rps16 intron) and nuclear [internal transcribed spacer (ITS)1 and 5S-non-transcribed spacer (NTS)] DNA sequence data. The results show that two Asian genera, Halopegia and Stachyphrynium, are well-defined monophyletic entities that should be maintained in their current form. Schu- mannianthus virgatus is sister to Halopegia and should be transferred to a genus of its own. Phacelophrynium, Monophrynium and Cominsia are nested within a paraphyletic Phrynium. Within this large clade, a number of geographically focused monophyletic species groups can be identified, in some cases corroborated by flower and fruit characters not previously emphasized in taxonomic studies, but these do not provide a useful framework for a revised generic classification. A revised generic classification of Asian Marantaceae is supplied, including the description of a new genus Indianthus Suksathan & Borchs. to which S. virgatus is transferred. © 2009 The Linnean Society of London, Botanical Journal of the Linnean Society, 2009, 159, 381–395. ADDITIONAL KEYWORDS: 5S-non-transcribed spacer (NTS) – internal transcribed spacer (ITS)1 – Malesia – nuclear DNA – plastid DNA – rps16 intron – Zingiberales. INTRODUCTION Other synapomorphies include leaf venation with sigmoid secondary veins and evenly spaced cross Marantaceae are a family of rhizomatous ground veins and the presence of a specialized pulvinus on herbs with a pantropical distribution comprising the junction between the leaf blade and the petiole c. 550 species in 31 genera (Andersson, 1998). From that enables the leaf blade to change position accord- both molecular and morphological evidence, it has ing to intensity and angle of the sunlight. been shown that the family forms a monophyletic In Asia, the family comprises c. 55 species in eight lineage with Cannaceae as sister group (Dahlgren genera. They are found in lowland and montane rain- & Rasmussen, 1983; Kress, 1990; Smith, Kress & forests from sea level up to an altitude of 1700 m, Zimmer, 1993; Kress et al., 2001). The flower struc- ranging from India eastward to the South Pacific ture is highly complex within the family. Flowers are islands (Vanuatu), including New Guinea and the asymmetric, with specialized staminodial structures Philippines, with the highest species diversity occur- adapted to facilitate an advanced pollination system ring in Borneo (c. 20 spp.). Until recently, the Asian in which the style is held under tension and released Marantaceae were very poorly known relative to upon contact with a visiting insect (Kennedy, 1977). their Neotropical counterparts (Andersson, 1986; Kennedy, 1986; Andersson, 1998), but several recent *Corresponding author. contributions have helped clarify alpha-taxonomy E-mail: fi[email protected] (e.g. Clausager & Borchsenius, 2003; Suksathan & © 2009 The Linnean Society of London, Botanical Journal of the Linnean Society, 2009, 159, 381–395 381 382 P. SUKSATHAN ET AL. Borchsenius, 2003; Poulsen & Clausager, 2004; and Sanblasia) not represented] using sequence data Suksathan & Borchsenius, 2005; Clausager, Mood for three plastid DNA regions (matK and adjoining 3′ & Borchsenius, 2006; Suksathan, Borchsenius & matK-trnK intergenic spacer; trnL-trnF intergenic Poulsen, 2006; Suksathan & Borchsenius, 2008). spacer). That study identified five major clades within Generic delimitation and phylogenetic relationships the family, three of which have Asian representatives: between genera, however, remain unclear. The most the Stachyphrynium clade (Stachyphrynium); the comprehensive systematic treatment of the family Maranta clade [Halopegia, Schumannianthus virga- produced to date is the monograph by Schumann tus (Roxb.) Rolfe] and the Donax clade [remaining (1902). In this work, the Asian taxa were referred to Asian genera plus Schumannianthus dichotomus eight different genera: Actoplanes K. Schum. (= Donax (Roxb.) Gagnep.]. Problems with generic delimitation Lour.), Cominsia Hemsl., Donax (= Schumannianthus were detected in two cases: Schumannianthus was Downloaded from https://academic.oup.com/botlinnean/article/159/3/381/2418341 by guest on 02 October 2021 Gagnep.), Halopegia K. Schum., Monophrynium K. found to be polyphyletic and Phacelophrynium was Schum., Phacelophrynium K. Schum., Phrynium nested within Phrynium. The analysis, however, Willd. and Stachyphrynium K. Schum. Since then, included only a single species of Phacelophrynium. generic concepts have remained essentially unalt- Prince & Kress (2006b) found the same five major ered (Andersson, 1998) and only nomenclature has clades in an analysis of a more limited taxon sample changed. but including data from eight DNA regions represent- The Marantaceae have traditionally been divided ing the plastid (matK, ndhF, rbcL, rps16 intron and into two tribes: Phrynieae Petersen with three fertile trnL-trnF intergenic spacer), mitochondrial (cox1) and ovary locules and Maranteae Meisn. with one fertile nuclear genomes [internal transcribed spacer (ITS) ovary locule (Petersen, 1889). An alternative classifi- region and the 5′-end of 26S]. cation was proposed by Andersson (1998), who divided In this paper, we present a densely sampled phy- the family into five informal groups based on inflo- logeny for Asian Marantaceae based on a combination rescence and floral structures: the Phrynium, of plastid and nuclear DNA sequences. The taxon Calathea, Donax, Maranta and Myrosma groups. sample covers all Asian genera and more than 75% of According to this classification, the SE Asian genera the species currently known from that continent, belonged to two different groups: (1) the Phrynium several represented by more than one accession. The group (Phrynium, Monophrynium, Phacelophrynium specific objectives of the study were (1) to reconfirm and Stachyphrynium), characterized by flower groups the position of the Asian members within the family (‘cymules’) with strongly condensed axes (brachy- using a large taxon sample and (2) to address the blastic) or with slightly extended axes (moderately unsettled questions concerning generic delimitation dolichoblastic), bracteole absent, interphylls usually using a combination of plastid and nuclear genome present, corolla tube short or long and 1–2 outer markers. staminodes; and (2) the Donax group (Donax and Schumannianthus), characterizd by flower groups with extended axes, interphyll absent, a small, glan- MATERIAL AND METHODS dular bracteole present, corolla tube short (rarely TAXON SAMPLING AND DATASETS moderately long) and two outer staminodes. Two Forty-eight Asian and five non-Asian Marantaceae Asian genera, Halopegia and Cominsia, were left by samples were sequenced for the plastid rps16 intron, Andersson as ‘genera of uncertain affinity’. nuclear ITS1 and 5S-non-transcribed spacer (NTS). Andersson & Chase (2001) published the first For the rps16 intron, we additionally downloaded densely sampled phylogenetic study of Marantaceae, sequences for 42 Marantaceae and ten other members including both morphological and molecular data of Zingiberales from GenBank. Most of these (plastid DNA rps16 intron) for 59 species of Maran- sequences form part of the data set studied by Ander- taceae in 21 genera. The results showed that neither sson & Chase (2001). Finally, one additional non- the traditional subdivision of Marantaceae into a trio- Asian sample [Marantochloa filipes (Benth. & Hook. vulate (Phrynieae) and uniovulate (Maranteae) tribe f.) Hutch.] was sequenced for the rps16 intron and (Petersen, 1889) nor the five informal groups pro- included in the family level analysis. A complete list posed by Andersson (1998) were natural. Only the of plant accessions, voucher specimens and GenBank Calathea and Myrosma groups were monophyletic, accession numbers is given in Table 1. The data were the Maranta and Phrynium groups were polyphyletic organized into three datasets: and the Donax group formed a grade involving a number of independent evolutionary lineages within 1. Family level rps16 intron dataset, with sequence the family. Prince & Kress (2006a) analysed a larger data for 95 ingroup samples from the Marantaceae sample of taxa [80 accessions in 27 genera; only four (one of the 48 Asian samples failed to produce genera (Monophrynium, Monophyllanthe, Myrosma a useful rps16 intron sequence, see RESULTS), © 2009 The Linnean Society of London, Botanical Journal of the Linnean Society, 2009, 159, 381–395 ASIAN MARANTACEAE 383 Table 1. Source and GenBank accession numbers for sequences used in this
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